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Into the functional ecology of ectomycorrhizal communities: Environmental filtering of enzymatic activities
Journal of Ecology
Abstract
1. Characterizing the ecological processes driving the assembly and functional composition of ectomycorrhizal (ECM) fungal communities is an area of active research.
2. Here, we applied a trait-based framework to address whether and how environmental filtering and niche differentiation influence the diversity of ECM fungal enzymatic activities in two oak-dominated forest ecosystems. We hypothesized that fungal enzymatic activities and ECM community assembly are influenced by the availability of targeted resources in the surrounding soil.
3. We pinpointed a major influence of environmental filtering on ECM fungal taxonomic and functional composition. Contrasted taxonomic composition among forest ecosystems was linked to broad interspecific trait variation and entailed contrasted functional responses at community-level. Conversely, intraspecific trait variation contributed to community response within ecosystems. We characterized a strong relationship between enzymatic activities and targeted resource availability in surrounding soil, suggesting a functional role of the enzymes for the acquisition of these resources. Conversely, we did not find a significant influence of niche differentiation in ECM community assembly.
4. Synthesis. Heterogeneous distribution of soil resources drives a community-level functional response and determines the functional and taxonomic mosaic of ECM communities in forest ecosystems.
... Additional isotopic evidence from Cortinarius sporocarps further suggests that members of this genus obtain organic N from SOM (Hobbie and Högberg 2012), and field evidence reveals that the relative abundance of Cortinarius spp are positively correlated with Mn-peroxidase activity, a potent extracellular enzyme mediating the oxidation of SOM . Shifts in the morphological attributes of ECM hyphae associated with N foraging , Defrenne et al. 2019) as well as enzyme and culture assays , Lilleskov et al. 2002a, Pierre-Emmanuel et al. 2016 along soil N gradients also implicitly support the hypothesis that ECM communities vary in their capacity to forage for biochemically distinct N forms. In further accordance with this overall rationale, distinct ECM genera are generally dominant members of fungal communities in which quantities of inorganic N are high (Lilleskov et al. 2002b, Edwards and Zak 2010) and culture-based nutritional studies of particular taxa that occur with fidelity in high inorganic N soils reveal that they cannot degrade complex organic N bearing molecules , Lilleskov et al. 2002b, Wolfe et al. 2012). ...
... However, unlike plant leaf traits, for which ecophysiological measurements have illuminated the functional significance of persistent patterns of trait variation(Ackerly et al. 2002, Cornwell and Ackerly 2009), underlying traits influencing the establishment and persistence of distinct ECM communities across soil N gradients remain unknown.Variation in the N foraging traits of ECM fungi represents a long-standing but inadequately tested hypothesis explaining shifts in ECM community membership along soil N gradients. ECM fungi differentially evolved from free-living saprotrophic ancestors and thus likely differ in their capacity to obtain N bound in soil organic matter (N-SOM)(Abuzinadah & Read 1986;Kohler et al. 2015;Pierre- Emmanuel et al. 2016;. Heterogeneity in the capacity for ECM taxa to obtain N-SOM may act as a key axis governing the assembly of ECM communities across soil N gradients(Pellitier et al. in review, Read and Perez-Moreno 2003, Koide et al. 2014). ...
... Heterogeneity in the capacity for ECM taxa to obtain N-SOM may act as a key axis governing the assembly of ECM communities across soil N gradients(Pellitier et al. in review, Read and Perez-Moreno 2003, Koide et al. 2014). Shifts in the morphological attributes of ECM hyphae associated with N foraging(Pellitier et al. in review, Moeller et al. 2014, Defrenne et al. 2019) as well as enzyme and culture assays, Lilleskov et al. 2002a, Bödeker et al. 2014a, Pierre-Emmanuel et al. 2016 along soil N gradients, implicitly support the hypothesis that ECM communities vary in their capacity to forage for biochemically distinct N forms. However, support for this hypothesis would challenge the emergent paradigm that globally distributed ECM communities ...
This dissertation investigates the capacity for ectomycorrhizal fungi to obtain Nitrogen (N), organically bound in soil organic matter (N-SOM). In Chapter 1, I delineate the gene families involved in the decay of SOM, and study their distribution across the ~ 85 independent evolutionary lineages of ECM fungi. I provide evidence that the polyphyletic nature of the ECM lifestyle has resulted in considerable variation in their genetic potential to obtain N-SOM. In addition, I describe several untested physiological conditions that limit our understanding of the contribution of N-SOM to plant growth. In chapters 2 and 3, I study ECM communities arrayed across a natural soil fertility gradient in Northern Michigan using a standardized tree host (Quercus rubra L.). I develop and test a whole-plant resource allocation framework that explicitly considers the composition and function of ECM communities and their net effect on plant uptake of organic and inorganic forms of N at the ecosystem scale. In Chapter 2, I employ a trait-based shotgun metagenome enabled approach to study variation in the genomic potential of ECM communities to obtain N-SOM. Foremost, I gathered support for the hypothesis that soil inorganic N availability acts as an environmental filter structuring the assembly of ECM communities and their trait distributions. Specifically, I document that the community weighted mean (CWM) genomic decay potential of ECM communities is inversely correlated with soil inorganic N availability. Furthermore, I tested the hypothesis that Q. rubra inhabiting low inorganic N soils, obtain greater quantities of N-SOM than do Q. rubra occupying inorganic N rich soils, due to physiological variation in the attributes of their ECM symbionts. I scaled CWM gene counts by the number of ECM infected root-tips present on individual root-systems to document that Q. rubra inhabiting low inorganic N soils host greater composite quantities of ECM genes involved in decay. Chapter 3 incorporates dendrochronological tree core data, Bayesian plant growth modeling approaches and molecular characterization of ECM communities and associated foraging morphologies. I show that N-SOM is likely to bolster net primary productivity (NPP) in soils where inorganic N is relatively scarce due to compositional and functional variation of associated ECM communities. Moreover, I compile dendrochronological evidence that trees inhabiting low inorganic N soils, exhibit a positive response to nearly 40 years of increasing ambient [CO2]. Integrating functional attributes of ECM communities, provides supports for the hypothesized importance of organic N in the global fertilizing effect of CO2 on NPP. Because ECM fungi that can degrade N-SOM carry a high carbon cost to their plant host, my results highlight potential tradeoffs in the role of the ECM symbiosis across soil inorganic N gradients. By documenting that N-SOM is unlikely to ubiquitously contribute to plant growth, my dissertation provides unique support for theory of optimal plant N foraging; I suggest that shifts in the functional attributes of ECM communities represent a mechanistic basis for plant flexibility in nutrient foraging strategies. Together, my analyses offers unprecedented molecular insight into the physiology of ECM communities and extends a functional biogeographic perspective that clarifies widespread observations of consistent patterns of ECM community turnover. Finally, my work adds further mechanistic evidence that the plant CO2 fertilization response is predicated upon the capacity of their ECM symbionts to obtain N-SOM, and clarifies the heterogeneous response of ECM forests to eCO2.
... Evidence is accumulating that compatibility between soil chemistry and EM fungal nutrient acquisition traits, including extracellular enzyme activities and ion flux rates, is part of the environmental filter for EM fungal community assembly. This has been observed in forests with different host species [27], and over successional [28,29] and nitrogen (N) gradients [30]. Such congruence between functional traits and local edaphic conditions can arise through several mechanisms: species selection, adaptation of fungal populations to site conditions over time, or phenotypic plasticity (i.e., acclimation; [27]). ...
... This has been observed in forests with different host species [27], and over successional [28,29] and nitrogen (N) gradients [30]. Such congruence between functional traits and local edaphic conditions can arise through several mechanisms: species selection, adaptation of fungal populations to site conditions over time, or phenotypic plasticity (i.e., acclimation; [27]). Site-specific EM fungal communities possessing traits that increase access to growth-limiting nutrients are expected to contribute to the overall fitness of the plant partner and, hence, the symbiosis [31]. ...
... Through competition with other fungi and/or support by the tree, assembly of the Podzol EM fungal communities could have involved selection of either fungal species [77] or individual fungi within the population with appropriate Pacquisition traits, or acclimation of existing fungi to the low P i and high P o through upregulation of phosphatase genes. Given the high β diversity across this landscape, it appears less likely that capacity for physiological plasticity by fungal individuals or intraspecific variations were drivers of EM fungal community assembly here [27]. Some controlled, manipulative studies (e.g., reciprocal seedling transplants across soil types; [78]) could be used to test these capacities more thoroughly. ...
Ectomycorrhizal (EM) fungi can acquire phosphorus (P) through the production of extracellular hydrolytic enzymes (exoenzymes), but it is unclear as to the manner and extent native EM fungal communities respond to declining soil P availability. We examined the activity of six exoenzymes (xylosidase, N -acetyl glucosaminidase, β-glucosidase, acid phosphomonoesterase, acid phosphodiesterase [APD], laccase) from EM roots of Pseudotsuga menzesii across a soil podzolization gradient of coastal British Columbia. We found that APD activity increased fourfold in a curvilinear association with declining inorganic P. Exoenzyme activity was not related to organic P content, but at a finer resolution using ³¹ P-NMR, there was a strong positive relationship between APD activity and the ratio of phosphodiesters to orthophosphate of surface organic horizons (forest floors). Substantial increases (two- to fivefold) in most exoenzymes were aligned with declining foliar P concentrations of P . menzesii , but responses were statistically better in relation to foliar nitrogen (N):P ratios. EM fungal species with consistently high production of key exoenzymes were exclusive to Podzol plots. Phosphorus deficiencies in relation to N limitations may provide the best predictor of exoenzyme investment, reflecting an optimal allocation strategy for EM fungi. Resource constraints contribute to species turnover and the assembly of distinct, well-adapted EM fungal communities.
... communities change along natural gradients of site productivity (Kranabetter et al. 2009), age (LeDuc et al. 2013), soil moisture (Moeller et al. 2014), and elevation (Jarvis et al. 2015), even when the same tree species is the major plant symbiont along the gradient; these shifts in species composition relate to differences in utilization (Lilleskov et al. 2002) or uptake rates (Kranabetter et al. 2015a) of different forms of N at the community level. Such local adaptation has been used as evidence that environmental filtering acts as a major process in structuring mature EMF communities (Blaalid et al. 2014;Peršoh 2015;Courty et al. 2016). ...
... More recently, molecular studies have confirmed that the presence and number of genes for organic matterdegrading enzymes vary in the genomes of EMF species (Bödeker et al. 2009;Floudas et al. 2012;Kohler et al. 2015). Nevertheless, environmental factors can also strongly influence the EEAs associated with an ectomycorrhiza (Mosca et al. 2007;Jones et al. 2012;Courty et al. 2016). If the early-and late-successional EMF communities in our study displayed a high degree of acclimation to the new edaphic conditions (H2), we expected to see similar EEAs between the two communities in both transplant environments. ...
... Evidence has accumulated that EEAs vary together with EMF communities among edaphic environments: e.g., in limed vs. unlimed soils (Rineau and Garbaye 2009), decayed wood vs. mineral soils (Buée et al. 2007), N-enriched vs. unenriched soils (Lilleskov et al. 2011 and references therein), clearcuts vs. mature spruce/fir forests (Walker et al. 2016), along an alpine chronosequence (Welc et al. 2014), and between two types of oak forest (Courty et al. 2016). In each of these cases, one could reasonably conclude that differences in EEAs are evidence of environmental filtering for species physiologically adapted to specific edaphic niches. ...
After stand-replacing disturbance, regenerating conifer seedlings become colonized by different ectomycorrhizal fungi (EMF) than the locally adapted EMF communities present on seedlings in mature forests. We studied whether EMF species that colonized subalpine fir (Abies lasiocarpa) seedlings in clearcuts differed from those that colonized seedlings in adjacent mature forests with respect to mycorrhizoplane extracellular enzyme activities (EEAs) and N status of the seedlings. We tested two alternate hypotheses: (1) that EEAs would differ between the two EMF communities, with higher activities associated with forest-origin communities, and (2) that acclimation to soil environment was considerable enough that EEAs would be determined primarily by the soil type in which the ectomycorrhizas were growing. Naturally colonized fir seedlings were reciprocally transplanted between clearcuts and forests, carrying different EMF communities with them. EEAs were influenced more by destination environment than by EMF community. EEAs were as high in early-successional as in late-successional communities in both destination environments. Buds of clearcut-origin seedlings had the same or higher N contents as forest seedlings after a growing season in either environment. These results indicate that (i) symbiotic EMF and/or their associated microbial communities demonstrate substantial ability to acclimate to new field environments; (ii) the ability to produce organic matter-degrading enzymes is not a trait that necessarily distinguishes early- and late-successional EMF communities in symbiosis; (iii) early-successional EMF are as capable of supporting seedling N accumulation in forest soils as late-successional EMF; and (iv) disturbed ecosystems where early-successional EMF are present should have high resilience for organic matter degradation.
... In the Mediterranean, global warming induced increased durations and intensity of droughts, with consequences on tree survival (Coma et al., 2009), and modified rates of soil biochemical cycling, especially N and C mineralization . The changes in nutrients cycling due to reductions in soil moisture are known to affect soil micro-organisms activity, in particular enzyme production by filamentous fungi (Courty et al., 2016;Sardans and Peñuelas, 2005). As a consequence, understanding how soil micro-organisms communities will respond to increased ongoing climate change, and especially to drought, is crucial to understand the ability of forest ecosystem functions to be maintained in the future (Bardgett et al., 2008). ...
... Increased ectomycorrhizal richness on roots positively influenced the survival of eleven month-old Quercus ilex seedlings (Figure 3.5). This result may reflect the welldocumented links between taxonomic and functional diversities (Maherali and Klironomos, 2012), and suggests that higher ECM fungal diversity entails higher ECM functional diversity, and a facilitated access of diversified soil resources for species (Courty et al., 2016(Courty et al., , 2005. ...
Mediterranean forests are facing an increase in the intensity and duration of droughts due to climate change, with potentially severe consequences for tree mortality and regeneration dynamics. This thesis investigates the potential carry-over drought effects that may affect the establishment, performance and survival of holm oak (Quercus ilex L.) seedlings alongside physiological and epigenetic modifications in mature trees. Specifically, it explores (i) the effects of microhabitat and ectomycorrhizal colonization on the establishment and survival of seedlings, (ii) the effects of drought on the diversity and composition of fungal communities and the subsequent consequences on seedling survival, and (iii) the effects of drought on the epigenetic modifications and physiological responses manifested in mother trees, which have the potential to be adaptive and enhance seedling survival. This thesis represents an interdisciplinary approach combining epigenetics, biotic interactions and environmental effects in a long-term drought experiment (15 years) with a reduction of 29% in annual precipitation in a Q.ilex forest in the south of France. Our results showed that even though summer drought was the main cause of seedling mortality, the precipitation reduction treatment increased the survival of seedlings compared to ambient conditions. This unexpected result was related to an increase in the ectomycorrhizal richness and an increase of drought adapted ectomycorrhizal species under drier conditions. Mother trees presented acclimation responses to drought that were correlated to changes in the methylome which suggest a potential role of epigenetics regulating these responses and a potential intergenerational transmission. This thesis provides evidence of the remarkable resilience to drought stress of the Mediterranean forests species, where recurrent environmental fluctuations may have favoured the emergence of long-term adaptation legacies.
... At broad taxonomic scale, a more important enzymatic machinery for fungi is expected compared to bacteria explaining their succession during litter decomposition , while the importance of bacteria in soil enzyme activity has also been showed (Manoharan et al. 2017, López-Mondéjar et al. 2019. Several studies also indicate a variation in enzymatic investment within bacterial and fungal groups , Pierre-Emmanuel et al. 2016. Gram positive and Gram negative bacteria are considered as oligotrophic and copiotrophic respectively ). ...
... Isolation studies have reported differences in enzymatic traits among microbial taxa , Pierre-Emmanuel et al. 2016, supporting the possibility of a community composition effect on total enzyme activity in soils. However, in empirical studies directly measuring total enzymes activity in soil, the effect of community composition on enzymes activity has rarely been assessed after correction for the biomass effect . ...
Dans le contexte actuel du changement climatique et de l’augmentation de la fréquence et de l’intensité des épisodes climatiques extrêmes, une question centrale pour l’écologie scientifique est de comprendre les répercussions de ces changements sur le fonctionnement des écosystèmes. Les communautés microbiennes du sol contrôlent une grande partie des processus écosystémiques déterminant la circulation de l’énergie et des nutriments. Dans le cadre des agroécosystèmes se pose donc la question de l’influence des pratiques agricoles sur les communautés microbiennes du sol et sur leur aptitude à maintenir le fonctionnement des écosystèmes face au changement climatique. L’intensification écologique de l’agriculture a récemment été proposée comme une approche intégrant les processus écologiques dans la stratégie de gestion des agroécosystèmes, dans l’objectif d’optimiser leur fonctionnement et leur résilience. L’écologie fonctionnelle pourrait répondre à certains des enjeux posés par le changement climatique et l’intensification écologique de l’agriculture.Dans cette thèse, j’ai cherché à mobiliser le cadre conceptuel des traits fonctionnels pour apporter de nouveaux éléments de compréhension de l’influence de différentes modalités d’intensité de gestion d’agroécosystèmes prairiaux (gestion extensive, conventionnelle-intensive et écologiquement-intensive) : 1) sur les caractéristiques fonctionnelles des communautés microbiennes du sol; 2) sur la capacité de ces communautés microbiennes à maintenir le fonctionnement de l’écosystème face à des périodes de stress climatiques (résilience). Dans le cadre de ma thèse, trois expérimentations ont été réalisées en faisant varier le degré de contrôle des facteurs de gestion, le type de stress climatique et la durée de ces stress. S’appuyant sur des agroécosystèmes prairiaux répartis dans trois pays Européens (France, Suisse, Portugal), les résultats des deux premières expérimentations de cette thèse montrent que les communautés microbiennes des sols des prairies écologiquement-intensives disposent d’une plus faible capacité à maintenir les propriétés écosystémiques microbiennes durant les stress (faible résistance) mais disposent d’une meilleure capacité de récupération comparée aux communautés microbiennes des sols en gestion conventionnelle-intensive. Une autre étude montre que la gestion éco-intensive favorise des communautés microbiennes protéolytiques bénéfiques à l’assimilation de l’azote pour les plantes en conditions perturbés. L’étude des traits végétaux suggère que ces effets de la gestion sur la composition des communautés microbiennes et sur leur résilience passe par certains traits, notamment une augmentation de la richesse en phosphore des litières en gestion écologiquement-intensive. En effet ces traits fonctionnels des plantes semblent influencer les traits microbiens, favorisant des communautés microbiennes copiotrophes, caractérisées par un ratio azote:phospore faible de leur biomasse et un faible investissement dans la production d’enzymes extracellulaires, deux traits négatifs pour la résistance au stress mais favorisant une récupération rapide. Ainsi, ces deux expérimentations soulignent l’importance de la gestion des traits des plantes dans le contrôle des traits microbiens et de la résilience des écosystèmes au changement climatique. La troisième expérimentation a cherché à tester spécifiquement les effets d’un épisode de fertilisation minérale sur la résilience des communautés microbiennes à différents stress climatiques. Les résultats montrent que la fertilisation modifie la composition et les traits microbiens avec des répercussions négatives sur la stabilité de l’écosystème face à la sécheresse et à l’inondation.Mobilisant une approche par le concept de trait fonctionnel microbien, ce travail de thèse apporte de nouveaux éléments de compréhension des effets de l’intensité de gestion sur la résilience des écosystèmes prairiaux face aux stress climatiques.
... Nevertheless, the importance of bacterial enzyme activity in soils has been shown (Manoharan et al., 2017;López-Mondéjar et al., 2019). Several studies also indicate a variation in enzymatic investment within bacterial and fungal groups (Lladó et al., 2016;Pierre-Emmanuel et al., 2016). Gram positive and Gram negative bacteria are considered as oligotrophic and copiotrophic respectively (Fierer et al., 2007;Fanin et al., 2018). ...
... Studies isolating bacteria and fungi have reported differences in enzymatic traits among microbial taxa (e.g. Lladó et al., 2016;Pierre-Emmanuel et al., 2016), supporting the possibility of a community composition effect on enzyme activity in soils. However, in empirical studies directly measuring potential enzyme activity in soil, the effect of community composition on enzyme activity has rarely been assessed after correction for the microbial biomass effect (Kivlin et al., 2013). ...
The functional trait framework provides a powerful corpus of integrated concepts and theories to assess how environmental factors influence ecosystem functioning through community assembly. While common in plant ecology, this approach is under-used in microbial ecology. After an introduction of this framework in the context of microbial ecology and enzymology, we propose an approach 1) to elucidate new links between soil microbial community composition and microbial traits; and 2) to disentangle mechanisms underlying “total” potential enzyme activity in soil (sum of 7 hydrolase potential activities). We address these objectives using a terrestrial grassland ecosystem model experiment with intact soil monoliths from three European countries (Switzerland, France and Portugal) and two management types (Conventional-intensive and Ecological-intensive), subjected to 4 rain regimes (Dry, Wet, Intermittent and Normal) under controlled conditions in a common climate chamber. We found tight associations between proxies of microbial ecoenzymatic community-weighted mean traits (enzymatic stoichiometry and biomass-specific activity) and community composition, bringing new information on resource acquisition strategy associated with fungi, Gram positive and Gram negative bacteria. We demonstrate that microbial biomass explained most of the total enzyme activity before altered rain regimes, whereas adjustments in biomass-specific activity (enzyme activity per unit of microbial biomass) explained most variation under altered rain regime scenarios. Furthermore, structural equation models revealed that the variation of community composition was the main driver of the variation in biomass-specific enzyme activity prior to rain perturbation, whereas physiological acclimation or evolutionary adaptation became an important driver only under altered rain regimes. This study presents a promising trait-based approach to investigate soil microbial community response to environmental changes and potential consequences for ecosystem functioning. We argue that the functional trait framework should be further implemented in microbial ecology to guide experimental and analytical design.
... The knowledge of ecological processes driving ECM community composition has improved in recent years thanks to the use of molecular tools (Suz et al. 2014). However, the connection between community composition and function (i.e. the role of ECM fungi in ecosystem processes and biogeochemical cycling) is still a challenge in fungal ecology (Courty et al. 2016). In this sense, the use of functional traits should allow for a more mechanistic understanding of fungal ecology (Aguilar-Trigueros et al. 2015). ...
... Both functional complementarity (lack of overlap among species in the trait of interest) and redundancy (overlap) among ECM fungal species that coexist in a given ecological niche have been reported (Jones et al. 2010;Rineau and Courty 2011). However, the relationship between the abundance of an ECM species and its potential enzyme activity is still little understood (Courty et al. 2016). ...
Some plants that associate with ectomycorrhizal (ECM) fungi are also able to simultaneously establish symbiosis with other types of partners. The presence of alternative partners that may provide similar benefits may affect ECM functioning. Here we compared potential leucine-aminopeptidase (LA) and acid phosphatase (AP) enzyme activity (involved in N and P cycling, respectively) in ECM fungi of three hosts planted under the same conditions but differing in the type of partners: Pinus (ECM fungi only), Eucalyptus (ECM and arbuscular mycorrhizal -AM- fungi) and Acacia (ECM, AM fungi and rhizobial bacteria). We found that the ECM community on Acacia and Eucalyptus had higher potential AP activity than the Pinus community. The ECM community in Acacia also showed increased potential LA activity compared to Pinus. Morphotypes present in more than one host showed higher potential AP and LA activity when colonizing Acacia than when colonizing another host. Our results suggest that competition with AM fungi and rhizobial bacteria could promote increased ECM activity in Eucalyptus and Acacia. Alternatively, other host-related differences such as ECM community composition could also play a role. We found evidence for ECM physiological plasticity when colonizing different hosts, which might be key for adaptation to future climate scenarios.
... The composition of ECMF communities is known to strongly vary with biotic factors, including forest use and management (Azul et al. 2010), forest vegetation composition and activity (Štursová et al. 2016), and host genotype (Lamit et al. 2016). The main drivers of ECMF also include abiotic conditions, climatic factors (Mucha et al. 2018), and soil properties (Albornoz et al. 2016) or soil resources (Courty et al. 2016). The diversity and structure of Quercus ECMF communities have already been studied based on the ITS barcoding of ECM tips (Smith and Read 2008;Azul et al. 2010;Shi et al. 2011;Richard et al. 2011;Lancellotti and Franceschini 2013). ...
... However, in this study, neither different bioclimate regions nor climate variables were considered. Although several environmental conditions known to govern ECMF composition [e.g., soil features, soil properties (Albornoz et al. 2016) and resources (Courty et al. 2016)] were not evaluated in the present work, the influence of bioclimate and its components (precipitation and temperature) for shaping ECMF structure was revealed. Castro et al. (2010) and Jarvis et al. (2013) also described precipitation as a main driver of ECMF community composition. ...
Cork oak (Quercus suber L.) forests play an important ecological and economic role. Ectomycorrhizal fungi (ECMF) are key components for the sustainability and functioning of these ecosystems. The community structure and composition of ECMF associated with Q. suber in different landscapes of distinct Mediterranean bioclimate regions have not previously been compared. In this work, soil samples from cork oak forests residing in different bioclimates (arid, semi-arid, sub-humid, and humid) were collected and surveyed for ectomycorrhizal (ECM) root tips. A global analysis performed on 3565 ECM root tips revealed that the ECMF community is highly enriched in Russula, Tomentella, and Cenoccocum, which correspond to the ECMF genera that mainly contribute to community differences. The ECMF communities from the rainiest and the driest cork oak forests were distinct, with soils from the rainiest climates being more heterogeneous than those from the driest climates. The analyses of several abiotic factors on the ECMF communities revealed that bioclimate, precipitation, soil texture, and forest management strongly influenced ECMF structure. Shifts in ECMF with different hyphal exploration types were also detected among forests, with precipitation, forest system, and soil texture being the main drivers controlling their composition. Understanding the effects of environmental factors on the structuring of ECM communities could be the first step for promoting the sustainability of this threatened ecosystem.
... In our analyses of ECM enzyme stoichiometry and potential energetic trade-offs, only ECM fungi with the medium-distance smooth exploration type (Thelephoraceae) showed an increase in SOM-degrading potential relative to P acquisition. This is not surprising, since the Thelephoraceae tend to dominate in organic-rich soil horizons [18,60] and show some of the strongest potential activities of degradative enzymes [4,6,61,62]. In addition, studies have shown that when host plants allocate less C to their ECM fungi, either due to dormancy or defoliation, the relative activity of C-degrading enzymes increases significantly [17,55,63]. ...
... Such results are more typical of competitive interactions; that is, where certain ECM taxa pre-emptively colonized roots and utilized resources [64,65] owing to competition for spatial co-existence (a limited availability of root tips) or overlap in resource utilization (limited C availability). Alternatively, the abiotic conditions created by N fertilization may have selected for more closely-related taxa than expected by chance (environmental filtering [62]; e.g., members of the Russulaceae and Thelephoraceae dominated N-fertilized plots). However, additional studies are needed to distinguish between these explanations. ...
Rapid economic development and accelerated urbanization in China has resulted in widespread atmospheric nitrogen (N) deposition. One consequence of N deposition is the alteration of mycorrhizal symbioses that are critical for plant resource acquisition (nitrogen, N, phosphorus, P, water). In this study, we characterized the diversity, composition, and functioning of ectomycorrhizal (ECM) fungal communities in an urban-adjacent Pinus elliottii plantation under ambient N deposition (~24 kg N ha −1 year −1), and following N fertilization (low N, 50 kg N ha −1 year −1 ; high N, 300 kg N ha −1 year −1). ECM functioning was expressed as the potential activities of extracellular enzymes required for organic N (protease), P (phosphomonoesterase), and recalcitrant polymers (phenol oxidase). Despite high ambient N deposition, ECM community composition shifted under experimental N fertilization, and those changes were linked to disparate levels of soil minerals (P, K) and organic matter (but not N), a decline in acid phosphatase (AP), and an increase in phenol oxidase (PO) potential activities. Based on enzyme stoichiometry, medium-smooth exploration type ECM species invested more in C acquisition (PO) relative to P (AP) following high N fertilization than other exploration types. ECM species with hydrophilic mantles also showed higher enzymatic PO:AP ratios than taxa with hydrophobic mantles. Our findings add to the accumulating evidence that shifts in ECM community composition and taxa specialized in organic C, N, and P degradation could modulate the soil nutrient cycling in forests exposed to chronic elevated N input.
... Under normal conditions, microbes exhibit a balanced investment in enzymes related to C acquisition (hydrolytic and oxidative enzymes), N acquisition (chitinase and aminopeptidases), and P acquisition (phosphatases) [32], a pattern shown for both soils and sediments. Similar relations between N-and P-acquiring enzymes were established by Courty et al. [33] for EcM fungi; the activity of oxidative enzymes, which liberate organic N and P from organic matter, was also correlated with both N-and P-acquiring enzymes. However, coordination of enzymatic activities could be lost in cases of drastic changes in the supply of mineral nutrients, as in the case of N enrichment. ...
Globally, forests are impacted by atmospheric nitrogen (N) deposition, affecting their structure and functioning above and below ground. All trees form mutualistic root symbioses with mycorrhizal fungi. Of the two kinds of mycorrhizal symbioses of trees, the ectomycorrhizal (EcM) symbiosis is much more sensitive to N enrichment than the arbuscular mycorrhizal (AM) symbiosis. Due to increasing N deposition, significant declines in the richness and abundance of EcM fungal species and shifts in community composition and functional traits have been recorded. Under increasing N deposition, ectomycorrhizal forests usually show enhanced foliar mass fractions of N, reduced foliar mass fractions of phosphorus (P), and, consequently, an increasing imbalance in the foliar N:P stoichiometry, ultimately impacting tree performance. The question has been raised of whether, under conditions of high N deposition, EcM trees can select EcM fungi that are both tolerant to high N availability and efficient in the acquisition of P, which could to some extent mitigate the negative impact of N deposition on nutrient balances. Here we evaluate the literature for mechanisms through which certain EcM fungi could increase P acquisition under increased N loading. We find very little evidence that under N enrichment, EcM fungi that have on average higher P efficiency might be selected and thereby prevent or delay tree N:P imbalances. However, methodological issues in some of these studies make it imperative to treat this conclusion with caution. Considering the importance of avoiding tree N:P disbalances under N enrichment and the need to restore EcM forests that have suffered from long-term excess N loading, further research into this question is urgently required.
... The influence of abiotic filtering (e.g. soil properties and climatic conditions) on the fungal community depended on variations in resource availability and the adaptive ability of different fungal taxonomy (Courty et al., 2008;Pierre-Emmanuel et al., 2016). Additionally, competition among fungi derived priority effects also played a central role in determining fungal community assembly (Koide et al., 2005;Kennedy et al., 2009). ...
The semi-arid region of the Western Ordos plateau in Inner Mongolia, China, is home to a critically endangered shrub species, Potaninia mongolica, which originates from ancient Mediterranean regions. Root-associated microbiomes play important roles in plant nutrition, productivity, and resistance to environmental stress particularly in the harsh desert environment; however, the succession of root-associated fungi during the growth stages of P. mongolica is still unclear. This study aimed to examine root-associated fungal communities of this relict plant species across three seasons (spring, summer and autumn) using root sampling and Illumina Miseq sequencing of internal transcribed spacer 2 (ITS 2) region to target fungi. The analysis detected 698 fungal OTUs in association with P. mongolica roots, and the fungal richness increased significantly from spring to summer and autumn. Eurotiales, Hypocreales, Chaetothyriales, Pleosporales, Helotiales, Agaricales and Xylariales were the dominant fungal orders. Fungal community composition was significantly different between the three seasons, and the fungal taxa at various levels showed biased distribution and preferences. Stochastic processes predominantly drove community assembly of fungi in spring while deterministic processes acted more in the later seasons. The findings revealed the temporal dynamics of root-associated fungal communities of P. mongolica, which may enhance our understanding of biodiversity and changes along with seasonal alteration in the desert, and predict the response of fungal community to future global changes.
... The astonishing diversity of fungi constantly comes in highly patchy communities of organisms at the local scale, with a large proportion of rarely observed taxa [20][21][22][23]. Long suspected to artefactually result from limited sampling efforts [20] which veils the realized communities [24], the high proportion of rare species in fungal communities was confirmed by analyses of mycelia, using the metabarcoding of either soil fractions [25,26] or plant fragments [27,28]. ...
Large datasets are highly valuable resources to investigate multi-scale patterns of organisms, and lay foundations for citizen science-based conservation strategies. Here, we used 1,043,262 records from 1708 to 2021 to explore the geography, taxonomy, ecology and distribution patterns of 11,556 fungal taxa in metropolitan France. Our analysis reveals a four-phase pattern of temporal recording, with a main contribution of post-1977 observations in relation with the structuration of associative mycology. The dataset shows an uneven geography of fungal recording. Four clusters of high-intensity sampling scattered across France contrast with poorly documented areas, including the Mediterranean. Basidiomycota and Agaricales highly dominate the dataset, accounting for 88.8 and 50.4% of records, respectively. The dataset is composed of many rare taxa, with 61.2% of them showing fewer than 100 records, and 20.5% recorded only once. The analysis of metadata brings to light a preponderance of the mycorrhizal guild (44.6%), followed by litter saprotrophs (31.6%) and wood saprotrophs (18.1%). Highly documented forests (76.3% of records) contrast with poorly investigated artificial (6.43%) and open habitats (10.1%). This work provides the first comprehensive overview of fungal diversity in France and identifies the Mediterranean area and open habitats as priorities to integrate into a global strategy for fungal conservation in France.
... The mechanisms underlying this pattern remains unclear. Saprotrophic fungi acquire their nutrients from inert organic matter, especially from tree litter and dead wood (Smith and Read 2010) lying on forest floor, and are then particularly exposed to environmental fluctuation, as well as to the highly variable availability and recalcitrant nature of soil organic matter (Courty et al., 2016) by comparison to ectomycorrhizal species. Alternatively, this result may reflect differences in fruit body size between saprotrophic and ectomycorrhizal species, and then differential carbon cost for reproductive investment between trophic modes (Bässler et al., 2015). ...
Long-term responses in the phenology of Mediterranean macrofungi to climatic changes are poorly documented. Here, we address this issue by comparing the fruiting patterns of 159 fungal species in Southern France between the first half of the 19th century and the first decade of the 21st century. We used a trait-based approach to assess the influence of phenology and morphology of fungal fruit bodies and their site ecology and biogeography on the response to climate change. We show that early autumnal fruiters, epigeous species and species with affinities for cold climates now start to fruit on average 16.4, 17.3 and 17.3 d later compared to their emergence dates in the 19th century, while late fruiters, hypogeous species and Mediterranean-restricted species did not change their fruiting date. Among ecological guilds, saproxylic species and pine-associated mutualists delayed their autumnal emergence by 32.5 and 19.2 d, likely in response to a delayed rewetting of litter and woody debris after extended summer drought. Our results suggest that long-term climate warming in the Mediterranean was accompanied by contrasting changes in the emergence of fungal fruit bodies according to ecological guilds, sporocarp life-forms and forest types.
... Using fungal cultures of ECM in Petri dishes, Bending and Read (1996) found that this ability was low. However, their experiment was conducted with pure mycelium in Petri dishes without a host plant, while fungal enzyme production might be largely modified by the association with plants (Courty et al., 2016). Using ectomycorrhizal Betula tremuloides in mesocosms, Madritch and Lindroth (2015) observed that N recovery increased with tannin concentration. ...
Ectomycorrhizal and ericoid fungi are increasingly recognized for their capacity to break down soil organic matter and getting access to organic nitrogen (N). In many forest ecosystems proteins complexed by plant-produced tannins constitute a substantial amount of organic N. Yet, it is currently unknown to what extent these N sources are accessible to ectomycorrhizae and their associated plants.
In a pot experiment, we provided ectomycorrhizal pine (Pinus pinea) seedlings with exactly the same amount of N either in mineral form, as protein, or as two different tannin-protein complexes, formed with commercially available tannins or tannins isolated from pine leaf litter.
Over a period of 18 months, pine seedlings grew at least two times bigger in all N-treatments. However, growth and N acquisition were roughly two and three times larger, respectively, with mineral N or protein supply compared to tannin-protein complexes as the sole N source (no difference between the two different complexes). With tannin-protein complexes, pine seedlings allocated relatively more biomass into fine roots. In addition, the decrease in tissue N concentration in the tannin-protein complex treatments was lower in fine roots (30%) than in needles (53%).
Our results showed that tannins strongly influence N nutrition in ectomycorrhizal pine seedlings. Tannin-protein complexes are an accessible N source for ectomycorrhizal pine seedlings although they grew better with easier accessible N. The respective contributions of ectomycorrhizal fungi and other free or root-associated microorganisms in the breakdown of tannin protein complexes recquires further exploration. Tannin-protein complexes may be an important N source in ecosystems where organic nitrogen dominates, but the respective contributions of ectomycorrhizal fungi and other free or root-associated microorganisms in the breakdown of tannin protein complexes recquires further exploration.
... Biodiversity metrics based on species counts are commonly used to describe the fungal community structure. However, other community parameters that take into account similarities in the ecological niche of species, such as fungal trait patterns (López-García et al., 2018;Treseder and Lennon, 2015;Courty et al., 2016;Zanne et al., 2020) or phylogenetic relatedness of taxa (Pérez-Izquierdo et al., 2020a,b;Pérez-Valera et al., 2015;Rincón et al., 2014;Tedersoo et al., 2012a) are gaining in importance. ...
Forest soil fungal communities are extremely complex and diverse, and show a range of different lifestyles from saprotrophs, endophytes, pathogens, and mycorrhizal species. These belowground communities are differently distributed through space and time scales, and they are involved in key ecosystem processes such as plant community dynamics, belowground trophic interactions, and biogeochemical cycles. Through examples from different global forest ecosystems, we describe the principal abiotic and biotic factors, including natural disturbances, driving the assemblage of fungal communities in forest soils, as well as potential underlying mechanisms. We have selected research studies directed at understanding how soil fungi activities and interactions impact forest functioning and can influence the goods and services provided by these ecosystems. Finally, we show how anthropic factors shape fungal communities and, in return, how soil fungi can be better integrated in forest practices to improve ecosystem services in the upcoming decades.
... The way ECM fungi affect host trees (Allen et al., 2003), and the EMM production (Agerer, 2001) differ between ECM species. Additionally, their enzymatic capabilities vary widely between species (Velmala et al., 2014;Courty et al., 2016;Walker et al., 2016), as well as their life history strategies and resistance to disturbances (Cairney, 1999). Therefore, even with unchanged ECM fungal biomass, changes in the ECM fungal community composition can influence EMM production and functioning. ...
Ectomycorrhizal (ECM) fungi are key players in N cycling in coniferous forests, and forest management such as application of wood ash can affect their functionality. The aim of this study was to determine the effects of wood ash application on ECM fungal mycelial production, capacity to retain N, diversity and community composition. In-growth mesh bags were installed in control and treated plots. After 6 months, ¹⁵N labeled ammonium and nitrate were applied into the mesh bags, and 24 h later extramatrical mycelium (EMM) was extracted and analyzed. Wood ash had no effects on EMM in-growth, N retention capacity, diversity or community composition. In contrast, there were significant seasonal differences in the amount of EMM produced. These results demonstrate that applying up to 6 t ha⁻¹ of wood ash in this type of plantation forest is a safe management practice that does not increase N leaching or negatively affect ECM fungi.
... Across environments, variation in EMF functional traits may relate better to ecosystem processes than variation in EMF species composition because it informs how groups of species function and the extent that there is functional redundancy in species diversity (Koide et al., 2014;Hazard and Johnson, 2018). For instance, EMF functional traits such as enzymatic activity (Courty et al., 2016), N preference (Leberecht et al., 2015;Haas et al., 2018), mycelial hydrophobicity or the differentiation of extraradical hyphae (i.e., exploration type; Agerer, 2001Agerer, , 2006Jarvis et al., 2013;Pickles et al., 2015a;Fernandez et al., 2017;Ostonen et al., 2017;Pena et al., 2017;Köhler et al., 2018;Rosinger et al., 2018) have been shown to impact ecosystem processes (Koide et al., 2014). Exploration type is a functional trait that connects the morphology and differentiation of EMF hyphae to differences in nutrient acquisition strategies. ...
Large-scale studies that examine the responses of ectomycorrhizal fungi across biogeographic gradients are necessary to assess their role in mediating current and predicted future alterations in forest ecosystem processes. We assessed the extent of environmental filtering on interior Douglas-fir (Pseudotsuga menziesii var. glauca (Beissn.) Franco) ectomycorrhizal fungal communities across regional gradients in precipitation, temperature, and soil fertility in interior Douglas-fir dominated forests of western Canada. We also examined relationships between fine-root traits and mycorrhizal fungal exploration types by combining root and fungal trait measurements with next-generation sequencing. Temperature, precipitation, and soil C:N ratio affected fungal community dissimilarity and exploration type abundance but had no effect on α-diversity. Fungi with rhizomorphs (e.g., Piloderma sp.) or proteolytic abilities (e.g., Cortinarius sp.) dominated communities in warmer and less fertile environments. Ascomycetes (e.g., Cenococcum geophilum) or shorter distance explorers, which potentially cost the plant less C, were favored in colder/drier climates where soils were richer in total nitrogen. Environmental filtering of ectomycorrhizal fungal communities is potentially related to co-evolutionary history between Douglas-fir populations and fungal symbionts, suggesting success of interior Douglas-fir as climate changes may be dependent on maintaining strong associations with local communities of mycorrhizal fungi. No evidence for a link between root and fungal resource foraging strategies was found at the regional scale. This lack of evidence further supports the need for a mycorrhizal symbiosis framework that is independent of root trait frameworks, to aid in understanding belowground plant uptake strategies across environments.
... It is possible that the dense hyphae characteristic of C. geophilum mycorrhizae led to higher measurements of root tip size and thus lower relative activity, but these hyphae would also create a much larger surface area. A recent study in French oak forests found that enzyme activity of C. geophilum varied significantly by site for five of eight enzymes tested, so context may be particularly important in determining enzyme activity of this taxon (Courty et al. 2016). ...
Common ecological restoration treatments such as thinning trees and prescribed burning could result in changes to soil fungal communities and changes to the function of those communities. Ecto-mycorrhizal fungi are especially likely to be affected as they are symbionts on plant roots and exhibit host and niche preferences. Ectomycorrhizal fungi also produce extracellular enzymes that are important in soil nutrient cycling. We conducted a community survey of ectomycorrhizal fungi and assayed ectomycor-rhizal root tip enzyme activity using substrate plugs in northern Mississippi upland oak-pine woodland plots differing in restoration history to explore the influence of woodland restoration on ectomycorrhizal fungal community composition and function. Restoration treatment was significant in explaining the occurrence of the most common fungal species (Russula xerampelina) and the most common family (Thele-phoraceae) in the ectomycorrhizal fungal community survey. Highest potential laccase, peroxidase, and N-acetyl-b-D-glucosaminidase enzyme activity were found in a prescribed burn plot, and the lowest enzyme activities at a wildfire plot, where richness of ectomycorrhizal fungi was also lower. Different fungal families displayed significantly different enzymatic capabilities, with Hydnangiaceae having the highest laccase activity and Tuberaceae having significantly higher peroxidase and chitinase activity than several other families. These results suggest that restoration treatments can affect ectomycorrhizal fungal community composition and function, and better understanding these changes can aid understanding of the niches of ectomycorrhizal fungi and the impacts of restoration.
... The diversity of EM assemblages also manifests in functional diversity, i.e., EM taxa exhibit differences in functional traits. Those functional traits and their effect on ecosystem functioning have received more and more attention in EM community ecology [17]. For example, considerable differences among taxa of EM fungi have been shown in terms of nutrient acquisition [18,19] and other functions, such as C costs for maintenance respiration [20]. ...
Ectomycorrhizal (EM) fungi are pivotal drivers of ecosystem functioning in temperate and boreal forests. They constitute an important pathway for plant-derived carbon into the soil and facilitate nitrogen and phosphorus acquisition. However, the mechanisms that drive ectomycorrhizal diversity and community composition are still subject to discussion. We investigated patterns in ectomycorrhizal diversity, community composition, and exploration types on root tips in Fagus sylvatica,Picea abies, and Pinus sylvestris stands across Europe. Host tree species is the most important factor shaping the ectomycorrhizal community as well as the distribution of exploration types. Moreover, abiotic factors such as soil properties, N deposition, temperature, and precipitation, were found to significantly influence EM diversity and community composition. A clear differentiation into functional traits by means of exploration types was shown for all ectomycorrhizal communities across the three analyzed tree species. Contact and short-distance exploration types were clearly significantly more abundant than cord- or rhizomorph-forming long-distance exploration types of EM fungi. Medium-distance exploration types were significantly lower in abundance than contact and short-distance types, however they were the most frequent EM taxa and constituted nearly half of the EM community. Furthermore, EM taxa exhibit distinct ecological ranges, and the type of soil exploration seemed to determine whether EM taxa have small or rather big environmental ranges.
... Among these ECM fungi, C. geophilum was more abundant in the pygmy terrace T3 compared to non-pygmy terrace T2 Moeller et al. 2014;this study). This taxon is well known for its ability to live in extreme environments, to resist to desiccation events, and to be dominant in weakly developed soils and for the production of protease and phosphatase activities (Pigott, 1982;Jany et al. 2003;Nygren et al. 2007;Obase et al. 2009;Courty et al. 2016;Peter et al. 2016). Consequently, C. geophilum may confer an advantage to the trees growing in the terrace T3 to deal with the low nutrient and water availability conditions. ...
Understanding how soil pedogenesis affects microbial communities and their in situ activities according to ecosystem functioning is a central issue in soil microbial ecology, as soils represent essential nutrient reservoirs and habitats for the biosphere. To address this question, soil chronosequences developed from a single, shared mineralogical parent material and having the same climate conditions are particularly useful, as they isolate the factor of time from other factors controlling the character of soils. In our study, we considered a natural succession of uplifted marine terraces in Mendocino, CA, ranging from highly fertile in the younger terrace (about 100,000 years old) to infertile in the older terraces (about 300,000 years old). Using ITS amplicon pyrosequencing, we analysed and compared the diversity and composition of the soil fungal communities across the first terraces (T1 to T3), with a specific focus in the forested terraces (T2 and T3) on soil samples collected below trees of the same species (Pinus muricata) and of the same age. While diversity and richness indices were highest in the grassland (youngest) terrace (T1), they were higher in the older forested terrace (T3) compared to the younger forested terrace (T2). Interestingly, the most abundant ectomycorrhizal (ECM) taxa that we found within these fungal communities showed high homology with ITS Sanger sequences obtained previously directly from ECM root tips from trees in the same study site, revealing a relative conservation of ECM diversity over time. Altogether, our results provide new information about the diversity and composition of the fungal communities as well as on the dominant ECM species in the soil chronosequence of Mendocino in relation to soil age and ecosystem development.
... Previous studies have attributed categorical trait information, usually extracted from databases, to each ECM fungal taxa (Aguilar-Trigueros et al., 2014;Kjøller et al., 2012) thereby ignoring the intraspecific variation and plasticity of these traits. As far as we know, only one recent study (Courty et al., 2016) has used direct trait characterisation of individual ECM root tips to develop a trait-based analysis. In that work, the authors demonstrated that extracellular enzyme traits at ECM fungal community level can be driven by the soil nutrient status. ...
Trait-based approaches are useful tools to explain ecological assembly rules and ecosystem functioning.
However, their use for soil microbiota has not been explored in depth yet. We explored trait-based functional
changes of ectomycorrhizal (ECM) fungal communities associated with holm oak (Quercus ilex subsp. ballota) in a
trace element contaminated area.
We found a variation in ECM fungal species composition determined by soil C, Ca and trace elements;
however, taxonomic diversity was not dependant on contamination level. Mean trait values of ECM fungal communities showed less rhizomorph and emanating hyphae production when increasing contamination, and the community converged towards species developing rhizomorphs less frequently. We suggest that trace elements in soils acted as the main environmental filter of trait diversity of ECM fungal communities. The effect of soil nutrients, i.e. soil C, affected the community mean trait values of emanating hyphae but did not cause a convergence in its distribution.
In summary, we found a reduction in the functional diversity of ECM fungal communities due to trace element contamination with potential to affect ecosystem functioning. This finding supports the potential of trait-based approaches to assess changes in the functional diversity of soil microbial communities.
... At a large spatial scale, covariation in functional traits and environmental variables, such as climate, should reveal the imprint of macroecological filters (functional biogeography, Violle et al. 2014). Although analysing the distribution of trait values in communities reveals major drivers of their assembly, the approach is still in its infancy in microbial ecology (but see Courty et al. (2016) for fungi and Kruk et al. (2010) for phytoplankton). We applied the framework to address the imprint of niche-based processes on the functional diversity of desmid communities in Europe. ...
Dispersal limitation, niche-based processes as well as historical legacies shape microbial biodiversity, but their respective influences remain unknown for many groups of microbes. We analysed metacommunity structure and functional trait variation in 148 communities of desmids, freshwater green algae, distributed throughout Europe. We delineated biogeographic modules for both taxa and sites using bipartite network analysis given that the taxa of a module co-occurred more often than expected by chance in sites of the same module. The network analysis distinguished two main acidic and neutral habitats, reflecting environmental filtering, and within each habitat separated species pools with distinct geographic locations, representing a plausible
influence of historical biogeography. The geographic differentiation was consistent with a hypothesis of glacial refugia on Atlantic coast. Distance decay in community composition in addition to environmental influence further suggested a role of dispersal limitation. Next, we quantified the variation in cell volume and surface-to-volume of taxa within and among communities, to examine morphological and physiological adaptations of desmids in varying environments. Communities from continental climate contained larger desmids. Conversely, we found a functional convergence of smaller, fast-growing, desmids in oceanic regions. Overall, our findings suggest that niche-based processes, dispersal limitation, and historical legacy together drive the distribution and structure of desmid communities. Combining trait- and network-based analyses can resolve long-lasting questions in microbial ecology and biogeography, and could be successfully used in macrobial ecology too.
... Previous studies have attributed ca- tegorical trait information, usually extracted from databases, to each ECM fungal taxa (Aguilar-Trigueros et al., 2014;Kjøller et al., 2012) thereby ignoring the intraspecific variation and plasticity of these traits. As far as we know, only one recent study (Courty et al., 2016) has used direct trait characterisation of individual ECM root tips to develop a trait-based analysis. In that work, the authors demonstrated that ex- tracellular enzyme traits at ECM fungal community level can be driven by the soil nutrient status. ...
Ectomycorrhizal (ECM) fungi associate with plants to conform one of the most important symbioses in terrestrial ecosystems, with important incidence in the provision of some ecosystem services. In 1998, a mine tailing spill affected an extensive area in the Guadiamar valley (Seville, Spain), causing a severe pollution by trace elements (TE). Remediation measures included top soil removal and amendments addition, followed by native tree species afforestation. Since then, monitoring activities have recorded several aspects of the biotic and abiotic conditions during the recovery of this degraded land, however, information about the soil organisms and their functional diversity is scarce. ECM fungal communities associated to planted holm oaks (Quercus ilex) were characterized both functional and taxonomically. We recorded 55 operational taxonomic units and found no differences in diversity between polluted and non-polluted plots. However the ECM fungal community composition was found to be dependent on soil characteristics such as pH, Ca and K content and to trace element concentrations. Functionally, a key trait for ecosystem functioning of ECM communities, the hyphal exploration type, was found to be dependent on the TE concentration in soil. This result points out the relevance of functional approaches when studying ecosystem restoration processes.
... These organisms also respond to biotic signals from their host under stressed conditions (Karst et al., 2014) or after disturbance (e.g. clear cutting; Jones et al., 2003), and from interactions between ECM fungal species (Courty et al., 2016). ...
... Tansley review New Phytologist Courty et al., 2016). Host plants may compete for these services provided by mycorrhizas (Walder et al., 2012(Walder et al., , 2015, which may also compete among themselves (Maherali & Klironomos, 2007;Yguel et al., 2014b). ...
Recent decades have seen declines of entire plant clades while other clades persist despite changing environments. We suggest that one reason why some clades persist is that species within these clades use similar habitats, because such similarity may increase the degree of co‐occurrence of species within clades. Traditionally, co‐occurrence among clade members has been suggested to be disadvantageous because of increased competition and enemy pressure. Here, we hypothesize that increased co‐occurrence among clade members promotes mutualist exchange, niche expansion or hybridization, thereby helping species avoid population decline from environmental change. We review the literature and analyse published data for hundreds of plant clades (genera) within a well‐studied region and find major differences in the degree to which species within clades occupy similar habitats. We tentatively show that, in clades for which species occupy similar habitats, species tend to exhibit increased co‐occurrence, mutualism, niche expansion, and hybridization – and rarely decline. Consistently, throughout the geological past, clades whose species occupied similar habitats often persisted through long time‐spans. Overall, for many plant species, the occupation of similar habitats among fellow clade members apparently reduced their vulnerability to environmental change. Future research should identify when and how this previously unrecognized eco‐evolutionary feedback operates.
Contents
Summary
66
I.
Entire clades decline while others persist; we suggest this might reflect an eco‐evolutionary feedback between habitat similarity among clade members, their co‐occurrence, and their reduced vulnerability to environmental change
67
II.
Definitions, and methods used to infer tentative evidence from published results
68
III.
The interface between variation in habitat use within clades and the assembly of local communities: clade members occupying similar habitats tend to locally co‐occur
69
IV.
The mainstream hypotheses in community ecology imply that co‐occurrence with fellow clade members is detrimental, but the evidence is equivocal
70
V.
We suggest that co‐occurrence with fellow clade members is often beneficial and we present evidence
73
VI.
There is tentative evidence for an eco‐evolutionary feedback between habitat similarity among clade members, their co‐occurrence, and their reduced vulnerability to environmental change
75
VII.
Conclusions and future directions
77
Acknowledgements
78
References
78
Land abandonment promotes forest expansion into abandoned agricultural lands in Europe. This process leads to changes that affect several ecosystem services, but it is considered a low‐cost strategy to restore soil functions in past agricultural lands. Soil microbial communities play a key role in restoring functions. However, the relationship among forest expansion, microbial communities, and soil functioning is unclear.
In this study, we used a Juniperus thurifera expansion gradient on abandoned agricultural lands in Alto Tajo National Park (Spain) to discover the changes elicited by the soil microbial communities and their functions along this gradient considering two microhabitats, under the canopy and open areas. Specifically, our objectives were (i) to analyse how soil properties (organic matter and pH), microbial communities (using PLFAs‐NFLAs) and enzymatic activities (related to C, N and P cycling) varied along the forest expansion gradient and between microhabitats and (ii) to decipher the pathways by which soil properties control the carbon and nutrient cycling in soils.
The forest expansion gradient had a direct negative effect on phosphatase activity. The microhabitat showed a positive direct effect on organic matter content, pH, actinomycetes and arbuscular mycorrhizal fungi biomass and on soil C and P cycling. Moreover, the biomass of gram‐positive bacteria determined the biomass of other microbial groups.
Synthesis and Applications: Though its effectiveness is variable, passive restoration can be more effective than active restoration. Our research indicates that passive tree colonisation of past agricultural land is enough to achieve soil functionality similar to a mature forest for most variables studied. However, some variables would need more time to reach mature forest levels, such as total microbial biomass and organic matter content. Therefore, to support ecosystem recovery, the management of this applied forest ecology strategy requires continuous monitoring of newly established trees and soil to elucidate the time needed to achieve mature soil properties.
Ectomycorrhizas (EcM) constitute a crucial component of soil biota in forest ecosystems, where they perform
functions of great ecological significance. Although there is available information about the individual effects of
various factors shaping EcM fungal communities, it is still challenging to understand the intricate interaction
among different environmental factors and forest management on these communities. Our aim was to evaluate
the potential modulation of silvicultural management impacts by site conditions on different facets of EcM fungal
biodiversity in mixed Nothofagus forests in northern Patagonia. We compared managed and unmanaged plots
located in mesic and humid sites, and assessed root colonization by EcM, taxonomic α- and β- EcM fungal diversity,
as well as relative abundance of functional EcM groups defined by fungal soil nutrient foraging strategies
(exploration types). We found that the effect of silvicultural management on root colonization was not modulated
by site conditions, being colonization percentages higher in the mesic site and in unmanaged plots. Conversely,
the effect of silvicultural management on taxonomic α- and β-diversity of EcM fungi, as well as on the relative
abundance of exploration types, was modulated by site conditions. We found that in the mesic site silvicultural
management tended to increase the α-diversity of EcM fungal communities and changed the relative abundance
of different EcM fungal taxa and EcM functional groups. In the humid site, silvicultural management did not
generate changes in α-diversity, but a shift in the relative abundance of certain EcM fungal taxa and of different
EcM functional groups was detected. These changes in taxonomic and functional EcM groups could be related to
the intrinsic traits of the EcM fungal species present in each site (e.g., stress tolerance, water, and nutrient
acquisition strategies) and how they interact with environmental disturbances, such as silvicultural management.
Overall, the composition of EcM fungi in all groups was affected by the interaction of both factors, although the
detected changes were mostly explained by modifications in the relative abundance of EcM fungi within each
group rather than species replacement terms. Our study highlights the complexity of ectomycorrhizas dynamics
in ecosystems and emphasizes the importance of considering belowground communities when analyzing the
impacts of silvicultural management. Furthermore, our results also reveal that silvicultural management
assessment and implementation should consider the environmental variation of the forest landscape.
Soil functioning is closely linked to the interactions between biological communities with the physical environment. Yet, the impact of plant community attributes on metabolic processes promoting soil nutrient cycling remains largely unknown. We hypothesized that the plant community acts as a regulating agent of nutrient mobilization in soils according to the phylogenetic and morpho-functional traits of plant species of which it is composed. Rhizosphere soils were collected in autumn and spring under 32 tree and shrub species in two Mediterranean mixed forests (four plots in each) located in southern Spain, and nine soil enzymatic activities related to C, N and P mobilization were assessed. Phylogeny and morpho-functional traits of plant species were recorded and their imprint in soil enzymatic activities across forests was determined. The results showed a plant phylogenetic signal for N mobilization in both forests, while it varied across forests for non-labile C and P mobilization. The plant phylogenetic signals were primarily driven by lineages that diversified through the Miocene, about 25 Myr ago. In addition, leaf traits and plant’s mycorrhizal type explained soil enzymatic activities independently from phylogeny. C and P mobilization increased under ectomycorrhizal plants, whilst enhanced N mobilization did occur under arbuscular mycorrhizal ones. The plant community composition led to a different carbon and nutrient mobilization degree, which in turn was mediated by distinct microbial communities mirroring differentiated resource-acquisition strategies of plants. Our results highlight the role of plant traits and mycorrhizal interactions in modulating carbon and nutrient cycling in Mediterranean mixed forest soils.
Trees acquire hydric and mineral soil resources through root mutualistic associations. In most boreal, temperate and Mediterranean forests, these functions are realized by a chimeric structure called ectomycorrhizae. Ectomycorrhizal (ECM) fungi are highly diversified and vary widely in their specificity toward plant hosts. Reciprocally, association patterns of ECM plants range from highly specialist to generalist. As a consequence, ECM symbiosis creates interaction networks, which also mediate plant–plant nutrient interactions among different individuals and drive plant community dynamics. Our knowledge of ECM networks essentially relies on a corpus acquired in temperate ecosystems, whereas the below-ground facets of both anthropogenic ECM forests and inter-tropical forests remain poorly investigated. Here, we successively (1) review the current knowledge of ECM networks, (2) examine the content of early literature produced in ECM cultivated forests, (3) analyze the recent progress that has been made in understanding the place of ECM networks in urban soils, and (4) provide directions for future research based on the identification of knowledge gaps. From the examined corpus of knowledge, we reach three main conclusions. First, the emergence of metabarcoding tools has propelled a resurgence of interest in applying network theory to ECM symbiosis. These methods revealed an unexpected interconnection between mutualistic plants with arbuscular mycorrhizal (AM) herbaceous plants, embedding ECM mycelia through root-endophytic interactions. This affinity of ECM fungi to bind VA and ECM plants, raises questions on the nature of the associated functions. Second, despite the central place of ECM trees in cultivated forests, little attention has been paid to these man-made landscapes and in-depth research on this topic is lacking. Third, we report a lag in applying the ECM network theory to urban soils, despite management initiatives striving to interconnect motile organisms through ecological corridors, and the highly challenging task of interconnecting fixed organisms in urban greenspaces is discussed. In particular, we observe a pauperized nature of resident ECM inoculum and a spatial conflict between belowground human pipelines and ECM networks. Finally, we identify the main directions of future research to make the needed link between the current picture of plant functioning and the understanding of belowground ECM networks.
The extent to which ectomycorrhizal (ECM) fungi decay soil organic matter (SOM) has implications for accurately predicting forest ecosystem response to climate change. Investigating the distribution of gene traits associated with SOM decay among ectomycorrhizal fungal communities could improve understanding of SOM dynamics and plant nutrition. We hypothesized that soil inorganic nitrogen (N) availability structures the distribution of ECM fungal genes associated with SOM decay and, specifically, that ECM fungal communities occurring in inorganic N‐poor soils have greater SOM decay potential.
To test this hypothesis, we paired amplicon and shotgun metagenomic sequencing of 60 ECM fungal communities associating with Quercus rubra along a natural soil inorganic N gradient.
Ectomycorrhizal fungal communities occurring in low inorganic N soils were enriched in gene families involved in the decay of lignin, cellulose, and chitin. Ectomycorrhizal fungal community composition was the strongest driver of shifts in metagenomic estimates of fungal decay potential. Our study simultaneously illuminates the identity of key ECM fungal taxa and gene families potentially involved in the decay of SOM, and we link rhizomorphic and medium‐distance hyphal morphologies with enhanced SOM decay potential.
Coupled shifts in ECM fungal community composition and community‐level decay gene frequencies are consistent with outcomes of trait‐mediated community assembly processes.
Plants associating with mutualistic ectomycorrhizal (ECM) fungi may directly obtain nitrogen (N) bound in soil organic matter (N-SOM). However, the contribution of N-SOM to plant growth under field conditions remains poorly constrained. We tested the hypothesis that turnover in ECM communities along soil inorganic N gradients mediates a functional transition from plant reliance on N-SOM in low inorganic N soils, to primarily inorganic N uptake in inorganic N-rich condition soils. We quantified the δ
15
N of Q. rubra foliage and roots, organic and inorganic soil N pools, and used molecular sequencing to characterize ECM communities, morpho-traits associated with N-foraging, and a community aggregated sporocarp δ
15
N. In support of our hypothesis, we document the progressive enrichment of root and foliar δ
15
N with increasing soil inorganic N supply; green leaves ranged from − 5.95 to 0.16‰ as the supply of inorganic N increased. ECM communities inhabiting low inorganic N soils were dominated by the genus Cortinarius, and other fungi forming hyphal morphologies putatively involved in N-SOM acquisition; sporocarp estimates from these communities were enriched (+ 4‰), further supporting fungal N-SOM acquisition. In contrast, trees occurring in high inorganic N soils hosted distinct communities with morpho-traits associated with inorganic N acquisition and depleted sporocarps (+ 0.5‰). Together, our results are consistent with apparent tradeoffs in the foraging cost and contribution of N-SOM to plant growth and demonstrate linkages between ECM community composition, fungal N-foraging potential and foliar δ
15
N. The functional characteristics of ECM communities represent a mechanistic basis for flexibility in plant nutrient foraging strategies. We conclude that the contribution of N-SOM to plant growth is likely contingent on ECM community composition and local soil nutrient availability.
Plant–soil feedbacks regulate plant productivity and diversity, but potential mechanisms underpinning such feedbacks, such as the allocation of recent plant assimilate, remain largely untested especially for plants forming tripartite symbioses.
We tested how soils from under alder Alnus glutinosa and beneath other species of the same and different families affected alder growth and nutrition, and colonization of roots by nitrogen‐fixing Frankia bacteria and ectomycorrhizal fungi. We also measured how the soil environment affected carbon capture and allocation by pulse labelling seedlings with ¹³CO2. We then tested for linkages between foliar nutrient stoichiometry and carbon capture and allocation and soil origin using statistical modelling approaches.
Performance of alder and nitrogen nutrition were best on home and birch Betula pendula soils (both Betulaceae), whereas performance on Douglas fir Pseudotsuga menziesii (Pinaceae) soil was poor. Plants growing in P. menziesii soil were virtually devoid of Frankia and ectomycorrhizas, and the natural abundance ¹⁵N signatures of leaves were more enriched indicating distinct nitrogen acquisition pathways. Seedlings in these soils also had smaller ¹³C fixation and root allocation rates, leading to smaller ¹³C respiration rates by microbes.
Statistical models showed that the best predictors of foliar N concentration were ¹³C allocation rates to fine roots and net CO2 exchange from the mesocosms. The best predictors for foliar phosphorus concentration were net CO2 exchange from the mesocosms and soil origin; seedlings in home soils tended to have greater foliar phosphorus compared to birch soils while seedlings from Douglas fir soils were no different from the other treatments. Foliar phosphorus concentration was not correlated with plant available or total soil phosphorus for any of the soils. Home soils also resulted in distinct ectomycorrhizal communities on seedlings roots, which could be responsible for greater foliar phosphorus concentration.
Our findings show how the association of alder with nitrogen‐fixing Frankia relieved nitrogen limitation in the seedling triggering a performance feedback loop. We propose that relief of nitrogen limitation likely increases plant phosphorus demand, which may promote the formation of ectomycorrhizas in nutrient‐deficient soils. The formation of tripartite symbioses therefore generates positive plant–soil feedbacks, which enables plants to acquire mineral nutrients otherwise inaccessible in trade for carbon.
A free Plain Language Summary can be found within the Supporting Information of this article.
As the Arctic rapidly warms, deciduous ectomycorrhizal (EcM) shrubs are expanding across the tundra. While we know how EcM host plants respond to warming and the associated nutrient release predicted for a future Arctic, considerably less is known about how EcM function will respond, despite their important role in plant nutrient acquisition in the nutrient-limited tundra. To explore how EcM-associated nutrient cycling may change, we characterized EcM-associated root enzyme activity and community in a 28-year full factorial warming and fertilization experiment in Arctic tundra. We measured activity at the individual root tip-level (pmol⋅min⁻¹⋅mm⁻² root) and used EcM root tip abundance to scale to community-level activity (pmol⋅min⁻¹⋅cm⁻³ soil). We then Sanger sequenced fungi on the same root tips to pair identity with function. Linear mixed effects models and multivariate analysis showed warming and fertilization generally had opposing, and sometimes interacting, effects on EcM root-associated activity. Responses also differed depending on the scale. Fertilization decreased activity on both scales while warming dampened the effect of fertilization. Additionally, warming increased EcM root tip abundance, and therefore community-level enzyme activity. Ectomycorrhizal root tip communities changed with fertilization, but not with warming. Changes in enzyme activity were moderately correlated with both changes in fungal community and soil inorganic nitrogen concentrations. The contrast in responses of root tip-level activity and community-level activity point to a potential shift in allocation to EcM function: whereas the production of degradative enzymes may become less important for nutrient acquisition, the exploration of the soil environment through increased number of EcM root tips may become more important. Furthermore, the future role of EcM in a warmer Arctic likely depends on the magnitude of nutrient release that comes with warming. While warming may increase the importance of EcM-associated nutrient cycling if nutrient availability remains low, it has the potential to decrease their importance if nutrient availability greatly increases.
Ectomycorrhizal (ECM) fungi form a symbiotic association with host trees, functionally promoting the nutrient uptake in the hosts via their secretion of enzymes to degrade organic compounds. Because of the involvement in nutrient cycling, ECM fungi are important to the establishment of host trees and forest recovery. In Thailand, ECM fungi are mostly associated with host tree species in the Dipterocarpaceae found in deciduous dipterocarp forests (DDFs), some of which are secondary forests naturally recovering after abandonment of logging and agriculture. To determine the function of ECM fungi in secondary DDFs, temporal changes in the ECM community structure and potential activities of three enzymes involved in nitrogen, carbon, and phosphorus cycling (β-N-acetylglucosaminidase, β-glucosidase, and acid phosphatase) from ECM roots and soils were investigated in two secondary DDF fragments in the Saraburi and Nan provinces of Thailand. A total of 180 soil samples from each forest were collected at four times across the wet and dry seasons from June 2015 to May 2016. Soil moisture content, total nitrogen, organic matter, and available phosphorus contents were measured. The results showed temporal changes in the ECM fungal communities and relative enzyme activities throughout the study period, although differences between the wet and dry seasons were not detected. The enzyme profiles associated with ECM roots were significantly correlated to the ECM communities in both DDFs. Moreover, the total nitrogen and soil moisture content influenced the temporal variation of ECM and soil enzyme profiles. These findings suggest the effect of edaphic factors combined with the ECM communities on their enzyme activities in secondary DDFs in Thailand.
Fire is a major disturbance linked to the evolutionary history and climate of Mediterranean ecosystems, where the vegetation has evolved fire‐adaptive traits (e.g., serotiny in pines). In Mediterranean forests, mutualistic feedbacks between trees and ectomycorrhizal (ECM) fungi, essential for ecosystem dynamics, might be shaped by recurrent fires. We tested how the structure and function of ECM fungal communities of Pinus pinaster and Pinus halepensis vary among populations subjected to high and low fire recurrence in Mediterranean ecosystems, and analyzed the relative contribution of environmental (climate, soil properties) and tree‐mediated (serotiny) factors. For both pines, local and regional ECM fungal diversity were lower in high than low fire recurrence areas, although certain fungal species were favored in the former. A general decline of ECM root‐tip enzymatic activity for Pinus pinaster was associated with high fire recurrence, but not for Pinus halepensis . Fire recurrence and fire related‐factors such as climate, soil properties or tree phenotype explained these results. In addition to the main influence of climate, the tree fire‐adaptive trait serotiny recovered a great portion of the variation in structure and function of ECM fungal communities associated with fire recurrence. Edaphic conditions (especially pH, tightly linked to bedrock type) were an important driver shaping ECM fungal communities, but mainly at the local scale and likely independently of the fire recurrence. Our results show that ECM fungal community shifts are associated with fire recurrence in fire‐prone dry Mediterranean forests, and reveal complex feedbacks among trees, mutualistic fungi and surrounding environment in these ecosystems.
To understand nutrient cycling in soils, soil processes and microorganisms need be better characterized. To determine whether specific trophic groups of fungi are associated with soil enzyme activity, we used soil imprinting to guide mm-scale sampling from microsites with high and low phosphatase activities in birch/Douglas-fir stands. Study 1 involved sampling one root window per site at 12 sites of different ages (stands); study 2 was conducted at one of the stem-exclusion stands, at which 5 root windows had been installed. Total fungal and ectomycorrhizal (EM) fungal terminal-restriction fragment length polymorphism (TRFLP) fingerprints differed between high- and low-phosphatase activity microsites at 8 of 12 root windows across 12 sites. Where differences were detected, fewer EM fungi were detected in high- than low-phosphatase activity microsites. Using 5 root windows at one site, next-generation sequencing detected similar fungal communities across microsites, but the ratio of saprotrophic to EM fungal reads was higher in high-phosphatase activity microsites in the two windows that had low EM fungal richness. In windows with differences in fungal communities, both studies indicated that EM fungi were less successful than saprotrophic fungi in colonizing fine-scale, organic matter-rich microsites. Fine-scale sampling linked with in situ detection of enzyme activity revealed relationships between soil fungal communities and phosphatase activity that could not be observed at the scales employed by conventional approaches, thereby contributing to the understanding of fine-scale phosphorus cycling in forest soils.
Seedlings that germinate after commercial harvesting are often colonized by the same early successional ectomycorrhizal fungi (EcM) as seen after wildfire. Because seedlings generally grow well with these fungi on disturbed sites for the first few years, there is no need for inoculation of seedlings being planted onto recently logged sites. To increase the spread of the later successional EcM fungi from intact forests, harvested areas should have high edge-to-area ratios achieved through aggregated retention harvest or smaller clearcuts. Planting diverse mixture of trees, leaving large pieces of downed wood, and avoiding compaction will help support a genetically diverse EcM fungal community in the regenerating stand. Neither thinning nor infrequent fertilization with moderate levels of a balanced fertilizer will cause major changes in EcM fungal communities or result in loss of organic matter-degrading ability. In order to maintain diverse EcM fungal communities, some old-growth stands should be maintained across the landscape.
Soils in boreal forests contain large stocks of carbon. Plants are the main source of this carbon through tissue residues and root exudates. A major part of the exudates are allocated to symbiotic ectomycorrhizal fungi. In return, the plant receives nutrients, in particular nitrogen from the mycorrhizal fungi. To capture the nitrogen, the fungi must at least partly disrupt the recalcitrant organic matterprotein complexes within which the nitrogen is embedded. This disruption process is poorly characterized. We used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ectomycorrhizal fungus Paxillus involutus degrades organic matter when acquiring nitrogen from plant litter. The fungus partially degraded polysaccharides and modified the structure of polyphenols. The observed chemical changes were consistent with a hydroxyl radical attack, involving Fenton chemistry similar to that of brown-rot fungi. The set of enzymes expressed by Pa. involutus during the degradation of the organic matter was similar to the set of enzymes involved in the oxidative degradation of wood by brown-rot fungi. However, Pa. involutus lacked transcripts encoding extracellular enzymes needed for metabolizing the released carbon. The saprotrophic activity has been reduced to a radical-based biodegradation system that can efficiently disrupt the organic matterprotein complexes and thereby mobilize the entrapped nutrients. We suggest that the released carbon then becomes available for further degradation and assimilation by commensal microbes, and that these activities have been lost in ectomycorrhizal fungi as an adaptation to symbiotic growth on host photosynthate. The interdependence of ectomycorrhizal symbionts and saprophytic microbes would provide a key link in the turnover of nutrients and carbon in forest ecosystems.
I. II. III. IV. V. VI. VII. References SUMMARY: Almost all land plants form symbiotic associations with mycorrhizal fungi. These below-ground fungi play a key role in terrestrial ecosystems as they regulate nutrient and carbon cycles, and influence soil structure and ecosystem multifunctionality. Up to 80% of plant N and P is provided by mycorrhizal fungi and many plant species depend on these symbionts for growth and survival. Estimates suggest that there are c. 50 000 fungal species that form mycorrhizal associations with c. 250 000 plant species. The development of high-throughput molecular tools has helped us to better understand the biology, evolution, and biodiversity of mycorrhizal associations. Nuclear genome assemblies and gene annotations of 33 mycorrhizal fungal species are now available providing fascinating opportunities to deepen our understanding of the mycorrhizal lifestyle, the metabolic capabilities of these plant symbionts, the molecular dialogue between symbionts, and evolutionary adaptations across a range of mycorrhizal associations. Large-scale molecular surveys have provided novel insights into the diversity, spatial and temporal dynamics of mycorrhizal fungal communities. At the ecological level, network theory makes it possible to analyze interactions between plant-fungal partners as complex underground multi-species networks. Our analysis suggests that nestedness, modularity and specificity of mycorrhizal networks vary and depend on mycorrhizal type. Mechanistic models explaining partner choice, resource exchange, and coevolution in mycorrhizal associations have been developed and are being tested. This review ends with major frontiers for further research.
© 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.
Significance
Microbes control vital ecosystem processes like carbon storage and nutrient recycling. Although megadiversity is a hallmark of microbial communities in nature, we still do not know how microbial diversity determines ecosystem function. We addressed this issue by isolating different geographic and local processes hypothesized to shape fungal community composition and activity in pine forests across the continental United States. Although soil enzyme activity varied across soils according to resource availability, enzyme activity was similar across different fungal communities. These observations indicate that much of fungal diversity plays an equal role in soil biogeochemical cycles. However, soil fungal communities vary dramatically in space, indicating that individual species are endemic to bioregions within the North American continent.
Soils of northern temperate and boreal forests represent a large terrestrial carbon (C) sink. The fate of this C under elevated atmospheric CO2 and climate change is still uncertain. A fundamental knowledge gap is the extent to which ectomycorrhizal fungi (EMF) and saprotrophic fungi contribute to C cycling in the systems by soil organic matter (SOM) decomposition. In this study, we used a novel approach to generate and compare enzymatically active EMF hyphae-dominated and saprotrophic hyphae-enriched communities under field conditions. Fermentation-humus (FH)-filled mesh bags, surrounded by a sand barrier, effectively trapped EMF hyphae with a community structure comparable to that found in the surrounding FH layer, at both trophic and taxonomic levels. In contrast, over half the sequences from mesh bags with no sand barrier were identified as belonging to saprotrophic fungi. The EMF hyphae-dominated systems exhibited levels of hydrolytic and oxidative enzyme activities that were comparable to or higher than saprotroph-enriched systems. The enzymes assayed included those associated with both labile and recalcitrant SOM degradation. Our study shows that EMF hyphae are likely important contributors to current SOM turnover in sub-boreal systems. Our results also suggest that any increased EMF biomass that might result from higher below-ground C allocation by trees would not suppress C fluxes from sub-boreal soils.The ISME Journal advance online publication, 31 October 2013; doi:10.1038/ismej.2013.195.
Although soil microorganisms play a central role in the soil processes that determine nutrient availability and productivity of forest ecosystems, we are only beginning to understand how microbial communities are shaped by environmental factors and how the structure and function of soil microbial communities in turn influence rates of key soil processes. Here we compare the structure and function of soil microbial communities in seven mature, undisturbed forest types across a range of regional climates in British Columbia and Alberta, and examine the variation in community composition within forest types. We collected the forest floor fermentation (F) and humus (H) layers and upper 10 cm of mineral soil at 3 sites in each of seven forest types (corresponding to seven Biogeoclimatic zones) in both spring and summer. Phospholipid fatty acid analysis was used to investigate the structure of soil microbial communities and total soil microbial biomass; potential activities of extra-cellular enzymes indicated the functional potential of the soil microbial community in each layer at each site.
Functional ecology aims at determining the relationships between species traits and environmental variables in order to better understand biological processes in ecosystems. From a methodological point of view, this biological objective calls for a method linking three data matrix tables: a table L with abundance or presence-absence values for species at a series of sites, a table R with variables describing the environmental conditions of the sites, and a table Q containing traits (e.g., morphological or behavioral attributes) of the species. Ten years ago, the fourth-corner method was proposed to measure and test the relationships between species traits and environmental variables using tables R, L, and Q simultaneously. In practice, this method is rarely used. The major reasons for this lack of interest are the restriction of the original method and program to presence-absence data in L and to the analysis of a single trait and a single environmental variable at a time. Moreover, ecologists often have problems in choosing a permutation model among the four originally proposed. In this paper, we revisit the fourth-corner method and propose improvements to the original approach. First, we present an extension to measure the link between species traits and environmental variables when the ecological community is described by abundance data. A new multivariate fourth-corner statistic is also proposed. Then, using numerical simulations, we discuss and evaluate the existing testing procedures. A new two-step testing procedure is presented. We hope that these elements will help ecologists use the best possible methodology to analyze this type of ecological problem.
An ectomycorrhiza is a multitrophic association between a tree root, an ectomycorrhizal fungus, free-living fungi and the associated bacterial communities. Enzymatic activities of ectomycorrhizal root tips are therefore result of the contribution from different partners of the symbiotic organ. However, the functional potential of the fungus-associated bacterial communities remains unknown. In this study, a collection of 80 bacterial strains randomly selected and isolated from a soil-ectomycorrhiza continuum (oak-Scleroderma citrinum ectomycorrhizas, the ectomycorrhizosphere and the surrounding bulk soil) were characterized. All the bacterial isolates were identified by partial 16S rRNA gene sequences as members of the genera Burkholderia, Collimonas, Dyella, Mesorhizobium, Pseudomonas, Rhizobium and Sphingomonas. The bacterial strains were then assayed for β-xylosidase, β-glucosidase, N-acetyl-hexosaminidase, β-glucuronidase, cellobiohydrolase, phosphomonoesterase, leucine-aminopeptidase and laccase activities, chitin solubilization and auxin production. Using these bioassays, we demonstrated significant differences in the functional distribution of the bacterial communities living in the different compartments of the soil-ectomycorrhiza continuum. The surrounding bulk soil was significantly enriched in bacterial isolates capable of hydrolysing cellobiose and N-acetylglucosamine. In contrast, the ectomycorrhizosphere appeared significantly enriched in bacterial isolates capable of hydrolysing glucopyranoside and chitin. Notably, chitinase and laccase activities were found only in bacterial isolates belonging to the Collimonas and Pseudomonas genera. Overall, the results suggest that the ectomycorrhizal fungi favour specific bacterial communities with contrasting functional characteristics from the surrounding soil.
Ecological communities and their response to environmental gradients are increasingly being described by various measures of trait composition. Aggregated trait averages (i.e. averages of trait values of constituent species, weighted by species proportions) are popular indices reflecting the functional characteristics of locally dominant species. Because the variation of these indices along environmental gradients can be caused by both species turnover and intraspecific trait variability, it is necessary to disentangle the role of both components to community variability. For quantitative traits, trait averages can be calculated from ‘fixed’ trait values (i.e. a single mean trait value for individual species used for all habitats where the species is found) or trait values for individual species specific to each plot, or habitat, where the species is found. Changes in fixed averages across environments reflect species turnover, while changes in specific traits reflect both species turnover and within-species variability in traits. Here we suggest a practical method (accompanied by a set of R functions) that, by combining ‘fixed’ and ‘specific averages’, disentangles the effect of species turnover, intraspecific trait variability, and their covariation. These effects can be further decomposed into parts ascribed to individual explanatory variables (i.e. treatments or environmental gradients considered). The method is illustrated with a case study from a factorial mowing and fertilization experiment in a meadow in South Bohemia. Results show that the variability decomposition differs markedly among traits studied (height, Specific Leaf Area, Leaf N, P, C concentrations, leaf and stem dry matter content), both according to the relative importance of species turnover and intraspecific variability, and also according to their response to experimental factors. Both the effect of intraspecific trait variability and species turnover must be taken into account when assessing the functional role of community trait structure. Neglecting intraspecific trait variability across habitats often results in underestimating the response of communities to environmental changes.
1. Trait-based approaches applied to community ecology have led to a considerable advance in understanding the effect of environmental filters on species assembly. Although plant traits are known to vary both between and within species, little is known about the role of intraspecific trait variability in the non-random assembly mechanisms controlling the coexistence of species, including habitat filtering and niche differentiation.
2. We investigate the role of intraspecific variability in three key functional traits – specific leaf area (SLA), leaf dry matter content (LDMC) and height – in structuring grassland communities distributed along a flooding gradient. We quantified the contribution of intraspecific variability relative to interspecific differences in the trait–gradient relationship, and we used a null model approach to detect patterns of habitat filtering and niche differentiation, with and without intraspecific variability.
3. Community mean SLA and height varied significantly along the flooding gradient and intraspecific variability accounted for 44% and 32%, respectively, of these trait–gradient relationships. LDMC did not vary along the gradient, with and without accounting for intraspecific variability. Our null model approach revealed significant patterns of habitat filtering and niche differentiation for SLA and height, but not for LDMC. More strikingly, considering intraspecific trait variability greatly increased the detection of habitat filtering and was necessary to detect niche differentiation processes.
4. Synthesis. Our study provides evidence for a strong role of intraspecific trait variability in community assembly. Our findings suggest that intraspecific trait variability promotes species coexistence, by enabling species to pass through both abiotic and biotic filters. We argue that community ecology would benefit from more attention to intraspecific variability.
Functional diversity is hypothesised as being beneficial for ecosystem functions, such as productivity and resistance to invasion. However, a precise definition of functional diversity, and hence a framework for its quantification, have proved elusive. We present a definition based on the analogy of the components of species diversity – richness, evenness and divergence. These concepts are applied to functional characters to give three components of functional diversity – functional richness, functional evenness and functional divergence. We demonstrate how each of these components may be calculated. It is hoped that our definition of functional diversity and its components will aid in elucidation of the mechanisms behind diversity/ecosystem-function relationships.
• Introduction
Many studies deal with taxonomic diversity (TD) or estimation of functional traits of ectomycorrhizal communities. However,
to our knowledge, none of them has ever tried to calculate the functional diversity (FD) of those communities, which is of
critical importance for the diversity and reliability of nutrient supply to the tree.
• Objectives
Here, we propose to evaluate the functional diversity of ECM communities in their potential ability to mobilise nutrients
from organic matter, in two different forest stands.
• Results
Results show that in both forest stands:
–
TD is strongly correlated with FD.
–
ECM species are functionally redundant within the communities for their abilities to secrete organic matter degrading enzymes.
–
The functional traits (enzymatic activities) of the studied ectomycorrhizal communities are not related within genera, nor
within families or phylogenetically related groups of taxa.
–
Some species show a wide phenotypic plasticity for their enzymatic profiles.
• Conclusion
This study provides the first evidence of functional redundancy in ectomycorrhizal communities. More studies are now needed
to evaluate the robustness of these results at wider ecosystem scales and using other relevant functional traits.
KeywordsEctomycorrhiza–Functional diversity–Functional redundancy–Functional plasticity–Functional traits–Taxonomic diversity
Soils in boreal forests contain large stocks of carbon. Plants are the main source of this carbon through tissue residues and root exudates. A major part of the exudates are allocated to symbiotic ectomycorrhizal fungi. In return, the plant receives nutrients, in particular nitrogen from the mycorrhizal fungi. To capture the nitrogen, the fungi must at least partly disrupt the recalcitrant organic matter-protein complexes within which the nitrogen is embedded. This disruption process is poorly characterized. We used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ectomycorrhizal fungus Paxillus involutus degrades organic matter when acquiring nitrogen from plant litter. The fungus partially degraded polysaccharides and modified the structure of polyphenols. The observed chemical changes were consistent with a hydroxyl radical attack, involving Fenton chemistry similar to that of brown-rot fungi. The set of enzymes expressed by Pa. involutus during the degradation of the organic matter was similar to the set of enzymes involved in the oxidative degradation of wood by brown-rot fungi. However, Pa. involutus lacked transcripts encoding extracellular enzymes needed for metabolizing the released carbon. The saprotrophic activity has been reduced to a radical-based biodegradation system that can efficiently disrupt the organic matter-protein complexes and thereby mobilize the entrapped nutrients. We suggest that the released carbon then becomes available for further degradation and assimilation by commensal microbes, and that these activities have been lost in ectomycorrhizal fungi as an adaptation to symbiotic growth on host photosynthate. The interdependence of ectomycorrhizal symbionts and saprophytic microbes would provide a key link in the turnover of nutrients and carbon in forest ecosystems.
Leaf-litter decomposition is a central process in carbon cycling; however, our knowledge about the microbial regulation of this process is still scarce. Metaproteomics allows us to link the abundance and activity of enzymes during nutrient cycling to their phylogenetic origin based on proteins, the 'active building blocks' in the system. Moreover, we employed metaproteomics to investigate the influence of environmental factors and nutrients on the decomposer structure and function during beech litter decomposition. Litter was collected at forest sites in Austria with different litter nutrient content. Proteins were analyzed by 1-D-SDS-PAGE followed by liquid-chromatography and tandem mass-spectrometry. Mass spectra were assigned to phylogenetic and functional groups by a newly developed bioinformatics workflow, assignments being validated by complementary approaches. We provide evidence that the litter nutrient content and the stoichiometry of C:N:P affect the decomposer community structure and activity. Fungi were found to be the main producers of extracellular hydrolytic enzymes, with no bacterial hydrolases being detected by our metaproteomics approach. Detailed investigation of microbial succession suggests that it is influenced by litter nutrient content. Microbial activity was stimulated at higher litter nutrient contents via a higher abundance and activity of extracellular enzymes.
Soils of coniferous forest ecosystems are important for the global carbon cycle, and the identification of active microbial decomposers is essential for understanding organic matter transformation in these ecosystems. By the independent analysis of DNA and RNA, whole communities of bacteria and fungi and its active members were compared in topsoil of a Picea abies forest during a period of organic matter decomposition. Fungi quantitatively dominate the microbial community in the litter horizon, while the organic horizon shows comparable amount of fungal and bacterial biomasses. Active microbial populations obtained by RNA analysis exhibit similar diversity as DNA-derived populations, but significantly differ in the composition of microbial taxa. Several highly active taxa, especially fungal ones, show low abundance or even absence in the DNA pool. Bacteria and especially fungi are often distinctly associated with a particular soil horizon. Fungal communities are less even than bacterial ones and show higher relative abundances of dominant species. While dominant bacterial species are distributed across the studied ecosystem, distribution of dominant fungi is often spatially restricted as they are only recovered at some locations. The sequences of cbhI gene encoding for cellobiohydrolase (exocellulase), an essential enzyme for cellulose decomposition, were compared in soil metagenome and metatranscriptome and assigned to their producers. Litter horizon exhibits higher diversity and higher proportion of expressed sequences than organic horizon. Cellulose decomposition is mediated by highly diverse fungal populations largely distinct between soil horizons. The results indicate that low-abundance species make an important contribution to decomposition processes in soils.
The species structure of an ectomycorrhizal (ECM) community was assessed monthly for 15 months in the two horizons (A1 and
A2) of an oak temperate forest in northeastern France. Ectomycorrhizal species were identified each month by internal transcribed
spacer sequencing. Seventy-five fungal symbionts were identified. The community was dominated by Tomentellaceae, Russulaceae,
Cortinariaceae, and Boletales. Four species are abundant in the study site: Lactarius quietus, Tomentella sublilacina, Cenococcum geophilum, and Russula sp1. The relative abundance of each species varied depending on the soil horizon and over time. Some species, such as L. quietus, were present in the A1 and A2 horizons. C. geophilum was located particularly in the A2 horizon, whereas T. sublilacina was more abundant in A1. Some species, such as Clavulina sp., were detected in winter, while T. sublilacina and L. quietus were present all year long. Our results support the hypothesis that a rapid turnover of species composition of the ECM community
occurs over the course of a month. The spatial and temporal unequal distribution of ECM species could be explained by their
ecological preferences, driven by such factors as root longevity, competition for resources, and resistance to environmental
variability.
Natural populations consist of phenotypically diverse individuals that exhibit variation in their demographic parameters and intra- and inter-specific interactions. Recent experimental work indicates that such variation can have significant ecological effects. However, ecological models typically disregard this variation and focus instead on trait means and total population density. Under what situations is this simplification appropriate? Why might intraspecific variation alter ecological dynamics? In this review we synthesize recent theory and identify six general mechanisms by which trait variation changes the outcome of ecological interactions. These mechanisms include several direct effects of trait variation per se and indirect effects arising from the role of genetic variation in trait evolution.
The aim of a joint effort by different research teams was to provide an improved procedure for enzyme activity profiling of field-sampled ectomycorrhizae, including recommendations on the best conditions and maximum duration for storage of ectomycorrhizal samples. A more simplified and efficient protocol compared to formerly published procedures was achieved by using manufactured 96-filter plates in combination with a vacuum manifold and by optimizing incubation times. Major improvements were achieved by performing the series of eight enzyme assays with a single series of root samples instead of two series, reducing the time needed for sample preparation, minimizing error-prone steps such as pipetting and morphotyping, and facilitating subsequent DNA analyses due to the reduced sequencing effort. The best preservation of samples proved to be storage in soil at 4-6 °C in the form of undisturbed soil cores containing roots. Enzyme activities were maintained for up to 4 weeks under these conditions. Short-term storage of washed roots and ectomycorrhizal tips overnight in water did not cause substantial changes in enzyme activity profiles. No optimal means for longer-term storage by freezing at -20 °C or storage in 100% ethanol were recommended.
Biota can be described in terms of elemental composition, expressed as an atomic ratio of carbon:nitrogen:phosphorus (refs 1-3). The elemental stoichiometry of microoorganisms is fundamental for understanding the production dynamics and biogeochemical cycles of ecosystems because microbial biomass is the trophic base of detrital food webs. Here we show that heterotrophic microbial communities of diverse composition from terrestrial soils and freshwater sediments share a common functional stoichiometry in relation to organic nutrient acquisition. The activities of four enzymes that catalyse the hydrolysis of assimilable products from the principal environmental sources of C, N and P show similar scaling relationships over several orders of magnitude, with a mean ratio for C:N:P activities near 1:1:1 in all habitats. We suggest that these ecoenzymatic ratios reflect the equilibria between the elemental composition of microbial biomass and detrital organic matter and the efficiencies of microbial nutrient assimilation and growth. Because ecoenzymatic activities intersect the stoichiometric and metabolic theories of ecology, they provide a functional measure of the threshold at which control of community metabolism shifts from nutrient to energy flow.
Knowledge of spatiotemporal patterns in species distribution is fundamental to understanding the ecological and evolutionary processes shaping communities. The emergence of DNA-based tools has expanded the geographic and taxonomic scope of studies examining spatial and temporal distribution of mycorrhizal fungi. However, the nature of spatiotemporal patterns documented and subsequent interpretation of ecological processes can vary significantly from study to study. In order to look for general patterns we synthesize the available data across different sampling scales and mycorrhizal types. The results of this analysis shed light on the relative importance of space, time and vertical soil structure on community variability across different mycorrhizal types. Although we found no significant trend in spatiotemporal variation among mycorrhizal types, the vertical community variation was distinctly greater than the spatial and temporal variability in mycorrhizal fungal communities. Both spatial and temporal variability of communities was greater in topsoil compared with lower horizons, suggesting that greater environmental heterogeneity drives community variation on a fine scale. This further emphasizes the importance of both niche differentiation and environmental filtering in maintaining diverse fungal communities.
We investigated the relationship between taxonomy and functioning of soil bacterial communities in soils from a Mediterranean holm oak forest using a high-throughput DNA pyrosequencing technique. We used nonparametric tests (Mann–Whitney U-test) to evaluate the sensitivity of each single bacterial genus within the community to the fluctuations of plant physiological and environmental abiotic variables, as well as to fluctuations in soil microbial respiration. Within-lineage (phylum/class) functional similarities were evaluated by the distribution of the Mann–Whitney U-test standardized coefficients (z) obtained for all genera within a given lineage. We further defined different ecological niches and within-lineage degree of functional diversification based on multivariate analyses (principal component analyses, PCA). Our results indicate that strong within-lineage functional diversification causes extensive functional overlapping between lineages, which hinders the translation of taxonomic diversity into a meaningful functional classification of bacteria. Our results further suggest a widespread colonization of possible ecological niches as taxonomic diversity increases. While no strong functional differentiation could be drawn from the analyses at the phylum/class level, our results suggest a strong ecological niche differentiation of bacteria based mainly on the distinct response of Gram-positive and Gram-negative bacteria to fluctuations in soil moisture.
We investigated the relation between taxonomy and functioning of soil bacterial communities in soils from a Mediterranean Holm-oak forest using a high throughput DNA pyrosequencing technique.
We investigated the relation between taxonomy and functioning of soil bacterial communities in soils from a Mediterranean Holm-oak forest using a high throughput DNA pyrosequencing technique.
Despite recent advances in understanding community ecology of ectomycorrhizal fungi, little is known about their spatial patterning and the underlying mechanisms driving these patterns across different ecosystems.
This meta‐study aimed to elucidate the scale, rate and causes of spatial structure of ectomycorrhizal fungal communities in different ecosystems by analysing 16 and 55 sites at the local and global scales, respectively. We examined the distance decay of similarity relationship in species‐ and phylogenetic lineage‐based communities in relation to sampling and environmental variables.
Tropical ectomycorrhizal fungal communities exhibited stronger distance‐decay patterns compared to non‐tropical communities. Distance from the equator and sampling area were the main determinants of the extent of distance decay in fungal communities. The rate of distance decay was negatively related to host density at the local scale. At the global scale, lineage‐level community similarity decayed faster with latitude than with longitude.
Synthesis . Spatial processes play a stronger role and over a greater scale in structuring local communities of ectomycorrhizal fungi than previously anticipated, particularly in ecosystems with greater vegetation age and closer to the equator. Greater rate of distance decay occurs in ecosystems with lower host density that may stem from increasing dispersal and establishment limitation. The relatively strong latitude effect on distance decay of lineage‐level community similarity suggests that climate affects large‐scale spatial processes and may cause phylogenetic clustering of ectomycorrhizal fungi at the global scale.
The relative contribution of top-down and bottom-up processes regulating primary decomposers can influence the strength of the link between the soil animal community and ecosystem functioning. Although soil bacterial communities are regulated by bottom-up and top-down processes, the latter are considered to be less important in structuring the diversity and functioning of fungal-dominated ecosystems. Despite the huge diversity of mycophagous (fungal-feeding) soil fauna, and their potential to reverse the outcomes of competitive fungal interactions, top-down grazing effects have never been found to translate to community-level changes. We constructed soil mesocosms to investigate the potential of isopods grazing on cord-forming basidiomycete fungi to influence the community composition and functioning of a complex woodland soil microbial community. Using metagenomic sequencing we provide conclusive evidence of direct top-down control at the community scale in fungal-dominated woodland soil. By suppressing the dominant cord-forming basidiomycete fungi, isopods prevented the competitive exclusion of surrounding litter fungi, increasing diversity in a community containing several hundred fungal species. This isopod-induced modification of community composition drove a shift in the soil enzyme profile, and led to a restructuring of the wider mycophagous invertebrate community. We highlight characteristics of different soil ecosystems that will give rise to such top-down control. Given the ubiquity of isopods and basidiomycete fungi in temperate and boreal woodland ecosystems, such top-down community control could be of widespread significance for global carbon and nutrient cycling.
Ectomycorrhizal ( ECM ) mycelium is a key component of the ectomycorrhizal symbiosis, yet we know little regarding the fine‐scale diversity and distribution of mycelium in ECM fungal communities.
We collected four 20 × 20 × 2‐cm ³ (800‐cm ³ ) slices of S cots pine ( P inus sylvestris ) forest soil and divided each into 100 2 × 2 × 2‐cm ³ (8‐cm ³ ) cubes. The presence of mycelium of ECM fungi was determined using an internal transcribed spacer ( ITS ) database terminal restriction fragment length polymorphism ( T ‐ RFLP ) approach.
As expected, many more ECM fungi were detected as mycelium than as ectomycorrhizas in a cube or slice. More surprisingly, up to one‐quarter of the 43 species previously detected as ectomycorrhizas over an area of 400 m ² could be detected in a single 8‐cm ³ cube, and up to three‐quarters in a single 800‐cm ³ slice. ECM mycelium frequency decreased markedly with depth and there were distinct ‘hotspots’ of mycelium in the moss/ F 1 layer.
Our data demonstrate a high diversity of ECM mycelium in a small (8‐cm ³ ) volume of substrate, and indicate that the spatial scale at which ECM species are distributed as mycelium may be very different from the spatial scale at which they are distributed as tips.
A lnus trees associate with ectomycorrhizal ( ECM ) fungi and nitrogen‐fixing F rankia bacteria and, although their ECM fungal communities are uncommonly host specific and species poor, it is unclear whether the functioning of A lnus ECM fungal symbionts differs from that of other ECM hosts.
We used exoenzyme root tip assays and molecular identification to test whether ECM fungi on A lnus rubra differed in their ability to access organic phosphorus ( P ) and nitrogen ( N ) when compared with ECM fungi on the non‐ F rankia host P seudotsuga menziesii .
At the community level, potential acid phosphatase ( AP ) activity of ECM fungal root tips from A . rubra was significantly higher than that from P . menziesii , whereas potential leucine aminopeptidase ( LA ) activity was significantly lower for A . rubra root tips at one of the two sites. At the individual species level, there was no clear relationship between ECM fungal relative root tip abundance and relative AP or LA enzyme activities on either host.
Our results are consistent with the hypothesis that ECM fungal communities associated with A lnus trees have enhanced organic P acquisition abilities relative to non‐ F rankia ECM hosts. This shift, in combination with the chemical conditions present in A lnus forest soils, may drive the atypical structure of A lnus ECM fungal communities.
There is a growing interest amongst community ecologists in functional traits. Response traits determine membership in communities. Effect traits influence ecosystem function. One goal of community ecology is to predict the effect of environmental change on ecosystem function. Environmental change can directly and indirectly affect ecosystem function. Indirect effects are mediated through shifts in community structure. It is difficult to predict how environmental change will affect ecosystem function via the indirect route when the change in effect trait distribution is not predictable from the change in response trait distribution. When response traits function as effect traits, however, it becomes possible to predict the indirect effect of environmental change on ecosystem function. Here we illustrate four examples in which key attributes of ectomycorrhizal fungi function as both response and effect traits. While plant ecologists have discussed response and effect traits in the context of community structuring and ecosystem function, this approach has not been applied to ectomycorrhizal fungi. This is unfortunate because of the large effects of ectomycorrhizal fungi on ecosystem function. We hope to stimulate further research in this area in the hope of better predicting the ecosystem-and landscape-level effects of the fungi as influenced by changing environmental conditions.
Soil extracellular enzymes are the proximal drivers of decomposition. However, the relative influence of climate, soil nutrients and edaphic factors compared to microbial community composition on extracellular enzyme activities (EEA) is poorly resolved. Determining the relative effects of these factors on soil EEA is critical since changes in climate and microbial species composition may have large impacts on decomposition. We measured EEA from five sites during the growing season in March and 17 sites during the dry season in July throughout southern California and simultaneously collected data on climate, soil nutrients, soil edaphic factors and fungal community composition. The concentration of carbon and nitrogen in the soil and soil pH were most related to hydrolytic EEA. Conversely, oxidative EEA was mostly related to mean annual precipitation. Fungal community composition was not correlated with EEA at the species, genus, family or order levels. The hyphal length of fungi was correlated with EEA during the growing season while relative abundance of taxa within fungal phyla, in particular Chytridiomycota, was correlated with the EEA of beta-glucosidase, cellobiohydrolase, acid phosphatase and beta-xylosidase in the dry season. Overall, in the dry season, 35.3 % of the variation in all enzyme activities was accounted for by abiotic variables, while fungal composition accounted for 27.4 %. Because global change is expected to alter precipitation regimes and increase nitrogen deposition in soils, EEA may be affected, with consequences for decomposition.
1. We sought evidence for limiting similarity, a basic aspect of community structure, in three zones of a saltmarsh. Sampling was conducted at three spatial scales (grains), from a single point up to the scale of several square metres. Twenty-three functional traits, related to the structure of the shoot and root systems and to nutrient status, were measured on each species present, separately in each community.
2. Patterns of association between plant species were compared with those expected under a null model, to assess whether plants with similar functional traits tended to coexist or to separate, i.e. whether there was environmental filtering or limiting similarity. A patch null model was used, a type that tends to be conservative but that avoids spurious evidence of limiting similarity caused by environmental pseudoreplication. One overall and four univariate test statistics were calculated, to capture possible patterns in trait space whilst minimising the problem of multiple testing.
3. In the Shrub community, overall evidence for even spacing of co-occurring species in functional-trait space, the pattern expected from the theory of limiting similarity, was seen at the area scale. In univariate tests in that community, there was evidence for even spacing in leaf lobation and leaf succulence, especially at small scales.
4. In the Rush community, there was significant evidence for limiting similarity in several traits, especially those related to canopy interactions, but also in some root characteristics. However, clustering in other traits, presumably owing to microenvironmental filtering, reduced overall tests for limiting similarity to ‘marginal significance’ (0.1 > P > 0.05).
5. In the species-poor and salt-stressed Salt turf, significant departures from the null model were sporadic and not consistent, although chlorophyll characters and leaf nitrogen concentration tended to be clustered.
6. Synthesis: There was evidence for niche limitation in two of the communities – Rush and Shrub – apparently based on canopy interactions in both cases and perhaps also root interactions in the latter community. Limiting similarity can be an important force in community assembly. However, in situations when it cannot be demonstrated, we do not know whether trait-based competition is absent or whether its signal is overwhelmed by other processes.
Ectomycorrhizal (ECM) fungi obtain both mineral and simple organic nutrients from soil and transport these to plant roots. Natural abundance of stable isotopes (¹⁵N and ¹³C) in fruit bodies and potential enzymatic activities of ECM root tips provide insights into mineral nutrition of these mutualistic partners. By combining rDNA sequence analysis with enzymatic and stable isotope assays of root tips, we hypothesized that phylogenetic affinities of ECM fungi are more important than ECM exploration type, soil horizon and host plant in explaining the differences in mineral nutrition of trees in an African lowland rainforest. Ectomycorrhizal fungal species belonging to extraradical mycelium-rich morphotypes generally displayed the strongest potential activities of degradation enzymes, except for laccase. The signature of ¹⁵N was determined by the ECM fungal lineage, but not by the exploration type. Potential enzymatic activities of root tips were unrelated to ¹⁵N signature of ECM root tip. The lack of correlation suggests that these methods address different aspects in plant nutrient uptake. Stable isotope analysis of root tips could provide an additional indirect assessment of fungal and plant nutrition that enables enhancement of taxonomic coverage and control for soil depth and internal nitrogen cycling in fungal tissues.
Summary • We sought evidence among the plant species of a New Zealand sand dune community that limiting similarity controls the ability of species to coexist. Sampling was at four spatial scales, from a single point up to a scale of 50 m2. Twenty-three functional characters were measured on each of the species, covering the morphology of the shoot and root systems and nutrient status, and intended to represent modes of resource acquisition. • Patterns of association between plant species at the four scales were examined for any tendency for plants with similar functional characters to coexist less often than expected at random (e.g. if a point has three species, do they have notably different characters?) The observed results were compared with the patterns expected under a null model using a range of test statistics. • A test over all characters found that the mean dissimilarity between nearest-neighbour species in functional space, and the minimum dissimilarity, were greater than expected under the null model at the 0.5 × 0.5 m scale. This supports the MacArthur & Levins model, although the actual community did not show an even spread of species over functional space. • Limiting similarity effects were seen even more consistently in separate characters when within-species variation was taken into account to calculate measures of overlap. The characters involved were mainly those related to rooting patterns and leaf water control, and thus perhaps reflecting the acquisition of nutrients and/or water. • Our results seem to be amongst the most convincing support for the theory of limiting similarity, and the only example involving vegetative processes in plant communities. The characters involved suggest that species can more readily coexist if they differ in their water-use pattern, reducing competition between them. Journal of Ecology (2004) 92, 557–567
In its simplest definition, a trait is a surrogate of organismal performance, and this meaning of the term has been used by evolutionists for a long time. Over the last three decades, developments in community and ecosystem ecology have forced the concept of trait beyond these original boundaries, and trait-based approaches are now widely used in studies ranging from the level of organisms to that of ecosystems. Despite some attempts to fix the terminology, especially in plant ecology, there is currently a high degree of confusion in the use, not only of the term “trait” itself, but also in the underlying concepts it refers to. We therefore give an unambiguous definition of plant trait, with a particular emphasis on functional trait. A hierarchical perspective is proposed, extending the “performance paradigm” to plant ecology. “Functional traits” are defined as morpho-physio-phenological traits which impact fitness indirectly via their effects on growth, reproduction and survival, the three components of individual performance. We finally present an integrative framework explaining how changes in trait values due to environmental variations are translated into organismal performance, and how these changes may influence processes at higher organizational levels. We argue that this can be achieved by developing “integration functions” which can be grouped into functional response (community level) and effect (ecosystem level) algorithms.
1. Clearcut logging results in major changes in ectomycorrhizal fungal communities, but whether this results in the loss of key functional traits, such as those associated with nutrient acquisition from soil organic matter, is unknown. Furthermore, little is known about the importance of resource partitioning in structuring ectomycorrhizal fungal communities following disturbance because most research on these communities has focussed on life history strategies. By studying functional traits, such as activities of enzymes involved in the catabolism of organic macromolecules in soil, we can determine whether a physiological potential for resource partitioning exists in pioneer ectomycorrhizal communities and whether severe disturbance affects these important ecosystem services.
2. We used activities of key hydrolytic enzymes in the ectomycorrhizospheres of Douglas‐fir seedlings regenerating at clearcut sites as a functional trait to test whether these differed from those at recent wildfire sites or control forests. We sampled the most abundant types of ectomycorrhizas from 16‐month‐old seedlings from sites exposed to (i) low or (ii) high severity wildfire, (iii) sites that had been clearcut logged in the same year as the fire and (iv) sites that contained control stands of mature Douglas‐fir. We expected differences in activities among ectomycorrhizas sampled from different disturbance treatments and among those formed by different fungal species.
3. In spite of large differences in soil chemistry, activities of acid phosphomonoesterase, N ‐acetylglucosaminidase and β‐glucosidase, when averaged among the ectomycorrhizas sampled per site, were not affected by disturbance agent. However, activities varied up to sixfold among mycorrhizospheres of different fungal species on the same seedling. Multivariate analysis also indicated some consistent differences in enzyme profiles among ectomycorrhizas formed by specific fungal species, independent of treatment.
4. The finding that ectomycorrhizal fungal communities exposed to different disturbance agents are functionally similar with respect to the activities of three mycorrhizosphere enzymes supports the conclusion that complementarity exists among ectomycorrhizal fungi. The substantial physiological diversity among ectomycorrhizal fungi at the scale of an individual seedling’s root tips, especially at control mature forests, indicates the potential for resource partitioning within the ectomycorrhizal community and access to a wider range of nutrient sources by each seedling.
5. Functional similarity among ectomycorrhizal fungal communities across a disturbance severity gradient suggests that dry interior Douglas‐fir forests are resilient to severe disturbances such as high severity wildfire and clearcutting with forest floor removal. Moreover, our results suggest that current harvesting practices emulate natural disturbances with respect to site‐level mycorrhizosphere enzyme activity. The large variation in activity among fungal species, however, indicates that a substantial simplification of the fungal community through other perturbations, as expected with climate change, has the potential to affect ecosystem function.
In landscapes subject to intensive agriculture, both soil fertility and vegetation disturbance are capable of impacting strongly, evenly and simultaneously on the herbaceous plant cover and each tends to impose uniformity on the traits of constituent species. In more natural and ancient grasslands greater spatial and temporal variation in both productivity and disturbance occurs and both factors have been implicated in the maintenance of species‐richness in herbaceous communities. However, empirical data suggest that disturbance is the more potent driver of trait differentiation and species co‐existence at a local scale. This may arise from the great diversity in opportunities for establishment, growth or reproduction that arise when the intensity of competition is reduced by damage to the vegetation.
In contrast to the diversifying effects of local disturbances, productivity‐related plant traits (growth rate, leaf longevity, leaf chemistry, leaf toughness, decomposition rate) appear to be less variable on a local scale. This difference in the effects of the productivity and disturbance filters arises from the relative constancy of productivity within the community and the diversity in agency and in spatial and temporal scales exhibited by disturbance events. Also, evolutionary responses to disturbances involve minor adaptive shifts in phenological and regenerative traits and are more likely to occur as micro‐evolutionary steps than the shifts in linked traits in the core physiology associated with the capacity to exploit productive and unproductive habitats.
During the assembly of a community and over its subsequent lifespan filters with diversifying and convergent effects may operate simultaneously on recruitment from the local species pool and impose contrasted effects on the similarity of the trait values exhibited by co‐existing species. Moreover, as a consequence of the frequent association of productivity with the convergence filter, an additional difference is predicted in terms of the effects of the two filters on ecosystem functioning. Convergence in traits selected by the productivity filter will exert effects on both the plant community and the ecosystem while divergent effects of the disturbance filter will be restricted to the plant community.
1. Ecologists and evolutionary biologists often need to simultaneously evaluate the significance of multiple related hypotheses. Multiple comparisons need to be corrected to avoid inappropriately increasing the number of null hypotheses that are wrongly rejected. The traditional method of correction involves Bonferroni‐type multiple comparison procedures which are highly conservative, tending to increase the number of wrong rejections of true hypotheses as the number of hypotheses being simultaneously tested increases.
2. Newer procedures which are based on False Discovery Rates and which do not suffer the same loss of power as traditional methods are described. Algorithms and spreadsheet‐based software routines for three procedures which are especially useful in ecology and evolution are provided.
3. The strengths and potential pitfalls of FDR‐based analysis and of presenting results as FDR‐adjusted P ‐values are discussed with reference to traditional methods such as the sequential Bonferroni correction.
4. FDR‐based multiple comparison procedures should be more widely adopted because they are often more appropriate than traditional methods for identifying truly significant results.
A leaf-height-seed (LHS) plant ecology strategy scheme is proposed. The axes would be specific leaf area SLA (light-capturing area deployed per dry mass allocated), height of the plant's canopy at maturity, and seed mass. All axes would be log-scaled. The strategy of a species would be described by its position in the volume formed by the three axes.The advantages of the LHS scheme can be understood by comparing it to Grime's CSR scheme, which has Competitors, Stress-tolerators and Ruderals at the corners of a triangle. The CSR triangle is widely cited as expressing important strategic variation between species. The C–S axis reflects variation in responsiveness to opportunities for rapid growth; in the LHS scheme, SLA reflects the same type of variation. The R axis reflects coping with disturbance; in the LHS scheme, height and seed mass reflect separate aspects of coping with disturbance.A plant ecology strategy scheme that permitted any species worldwide to be readily positioned within the scheme could bring substantial benefits for improved meta-analysis of experimental results, for placing detailed ecophysiology in context, and for coping with questions posed by global change. In the CSR triangle the axes are defined by reference to concepts, there is no simple protocol for positioning species beyond the reference datasets within the scheme, and consequently benefits of worldwide comparison have not materialized. LHS does permit any vascular land plant species to be positioned within the scheme, without time-consuming measurement of metabolic rates or of field performance relative to other species. The merits of the LHS scheme reside (it is argued) in this potential for worldwide comparison, more than in superior explanatory power within any particular vegetation region.The LHS scheme avoids also two other difficulties with the CSR scheme: (a) It does not prejudge that there are no viable strategies under high stress and high disturbance (the missing quadrant in the CSR triangle compared to a two-axis rectangle); (b) It separates out two distinct aspects of the response to disturbance, height at maturity expressing the amount of growth attempted between disturbances, and seed mass (inverse of seed output per unit reproductive effort) expressing the capacity to colonize growth opportunities at a distance.The advantage of LHS axes defined through a single readily-measured variable needs to be weighed against the disadvantage that single plant traits may not capture as much strategy variation as CSR's multi-trait axes. It is argued that the benefits of potential worldwide comparison do actually outweigh any decrease in the proportion of meaningful variation between species that is captured. Further, the LHS scheme opens the path to quantifying what proportion of variation in any other ecologically-relevant trait is correlated with the LHS axes. This quantification could help us to move forward from unprofitable debates of the past 30 years, where CSR opponents have emphasized patterns that were not accommodated within the scheme, while CSR proponents have emphasized patterns that the scheme did account for.
There is a need to quantify and qualify the ability of ectomycorrhizae to improve tree growth and nutrition and, in particular,
to define criteria to classify ectomycorrhizae with respect to ecologically relevant features. Whereas the numbers of ectomycorrhizae
and morphotypes give useful information when related to root biomass, root length or soil volume, the development and differentiation
of the extramatrical mycelium may represent important predicative features relevant to the ecological classification of ectomycorrhizae.
Here, different exploration types of ectomycorrhizae are distinguished based on the amount of emanating hyphae or the presence
and differentiation of rhizomorphs. Their putative ecological importance is discussed.