Article

Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal-temperate ecotone

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Abstract

Rising temperatures associated with climate change have been shown to negatively affect the photosynthetic rates of boreal forest tree saplings at their southern range limits. To quantify the responses of ectomycorrhizal (EM) fungal communities associated with poorly performing hosts, we sampled the roots of Betula papyrifera and Abies balsamea saplings growing in the B4Warmed (Boreal Forest Warming at an Ecotone in Danger) experiment. EM fungi on the root systems of both hosts were compared from ambient and +3.4 °C air and soil warmed plots at two sites in northern Minnesota. EM fungal communities were assessed with high-throughput sequencing along with measures of plant photosynthesis, soil temperature, moisture, and nitrogen. Warming selectively altered EM fungal community composition at both the phylum and genus levels, but had no significant effect on EM fungal operational taxonomic unit (OTU) diversity. Notably, warming strongly favored EM Ascomycetes and EM fungi with short-contact hyphal exploration types. Declining host photosynthetic rates were also significantly inversely correlated with EM Ascomycete and EM short-contact exploration type abundance, which may reflect a shift to less carbon demanding fungi due to lower photosynthetic capacity. Given the variation in EM host responses to warming, both within and between ecosystems, better understanding the link between host performance and EM fungal community structure will to clarify how climate change effects cascade belowground.

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... Exploration type could underlie EcM fungal species assembly (e.g. Castaño et al., 2018;Fernandez et al., 2017;Hobbie & Agerer, 2010;Moeller, Peay, & Fukami, 2014), but the mechanisms remain unresolved, with two competing hypotheses emerging. ...
... We refer to this as the 'functional offset' hypothesis, where ectomycorrhizas compensate for reductions in fine roots. Alternatively, the cost associated with the production of emanating tissues, by Distance mycorrhizas, may be prohibitive when carbon fixation is reduced, and thus Contact mycorrhizas dominate under those conditions (Castaño et al., 2018;Fernandez et al., 2017;Saikkonen et al., 1999;Saravesi, Markkola, Rautio, Roitto, & Tuomi, 2008). We refer to this as the 'energy-limited' hypothesis, where EcM fungi are independent agents responding to the supply of carbon. ...
... While relationships between LAI and number/proportion of Distance mycorrhizas were not statistically significant, we found indirect support for this hypothesis. Mean estimates of LAI and biomass growth were highest in the Mid age class, which suggests that these stands have the highest carbon supply and may explain the higher abundance of 'costly' Distance mycorrhizas (Castaño et al., 2018;Deslippe, Hartmann, Mohn, & Simard, 2011;Fernandez et al., 2017;Fransson, 2012). Conversely, mean LAI and biomass growth decreased in the Mature age class, suggesting that these stands may have less carbon available for mycorrhizal symbionts resulting in a lower abundance of Distance mycorrhizas. ...
Article
The abundance of fine roots and leaves in forests typically peaks during mid‐succession and then declines. If fine root area declines more rapidly than leaf area, this could contribute disproportionately to stand decline. However, trees also partner with symbiotic ectomycorrhizal (EcM) fungi that facilitate nutrient acquisition of fine roots. Ectomycorrhizal fungi can use the carbohydrates provided by their plant partners to produce emanating fungal tissues which increase soil exploration potential but may also prove costly. We suggest two competing hypotheses to frame the response of ectomycorrhizas to stand age: a) the ‘functional offset’ hypothesis posits that the abundance of ectomycorrhizas with emanating tissues (‘Distance’ mycorrhizas) increases with stand age, and b) the ‘energy‐limited’ hypothesis posits that carbon available for root symbionts decreases with stand age resulting in fewer Distance mycorrhizas. In the first hypothesis, EcM functional traits offset root abundance, while in the second, traits parallel root abundance. To test these competing hypotheses, we sampled fine roots to a depth of 90 cm and used allometric equations to estimate changes in root and leaf area index across a chronosequence of Pinus banksiana stands ranging from 2–76 years average tree age. We also examined fine roots microscopically to track changes in the abundance of EcM functional types. We used DNA‐based methods to sequence EcM fungi and confirm roots were of P.banksiana. Both fine root and leaf area of pine increased for the first 30–36 years (until Mid age) and then plateaued, while the ratio of leaf to fine root area was similar across the age gradient. Also, changes to fine root area with stand age depended on soil depth. The abundance of Distance mycorrhizas was lowest at the youngest plots and increased until Mid age, where it peaked, contrary to the functional offset hypothesis. Instead, the abundance of Distance mycorrhizas paralleled changes to leaf area, aligned with the energy‐limited hypothesis. Synthesis. Ectomycorrhizas do not offset the function of roots, rather shifts in exploration type likely reflect adjustments to carbon supply from hosts.
... This community shift appears to be attributable to certain fungal functional guilds being differentially sensitive to warming. For example, saprotrophic fungi have been shown to generally increase in relative abundance with warming (Treseder et al. 2016, Romero-Olivares et al. 2017, while the responses of ectomycorrhizal fungi are varied, being dependent on their hosts' growth and photosynthetic rates (Clemmensen et al. 2006, Fernandez et al. 2017. Our contrasting findings of decreased relative abundance of saprotrophic fungi with soil warming are potentially due to (1) competition with ectomycorrhizal fungi (Averill et al. 2014) as supported by an increased ratio of ectomycorrhizal to saprotrophic fungi in long-term warmed plots (2.33 AE 0.2) compared to control plots (0.70 AE 0.5), and/or (2) lower C concentrations and lignin relative abundance. ...
... Surprisingly, we found ectomycorrhizal fungi to be invariant to soil warming. Though global warming can alter the composition of ectomycorrhizal fungi by pushing them and/or their host plants outside their natural range of physiological tolerances (Kipfer et al. 2010, Fernandez et al. 2017, several other studies examining ectomycorrhizal response to increased temperatures have found small and/or absent effects (Parrent et al. 2006, Tu et al. 2015, Fernandez et al. 2017, Mucha et al. 2018. For example, in the boreal zone, ectomycorrhizal colonized tree species exposed to warming have shown a reduction in growth and photosynthetic rate , Fernandez et al. 2017, while warming of tree species in temperate zones has not resulted in similar reductions Oleksyn 2008, Wheeler et al. 2017). ...
... Surprisingly, we found ectomycorrhizal fungi to be invariant to soil warming. Though global warming can alter the composition of ectomycorrhizal fungi by pushing them and/or their host plants outside their natural range of physiological tolerances (Kipfer et al. 2010, Fernandez et al. 2017, several other studies examining ectomycorrhizal response to increased temperatures have found small and/or absent effects (Parrent et al. 2006, Tu et al. 2015, Fernandez et al. 2017, Mucha et al. 2018. For example, in the boreal zone, ectomycorrhizal colonized tree species exposed to warming have shown a reduction in growth and photosynthetic rate , Fernandez et al. 2017, while warming of tree species in temperate zones has not resulted in similar reductions Oleksyn 2008, Wheeler et al. 2017). ...
Article
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The direction and magnitude of climate warming effects on ecosystem processes such as carbon cycling remain uncertain. Soil fungi are central to these processes due to their roles as decomposers of soil organic matter, as mycorrhizal symbionts, and as determinants of plant diversity. Yet despite their importance to ecosystem functioning, we lack a clear understanding of the long‐term response of soil fungal communities to warming. Toward this goal, we characterized soil fungal communities in two replicated soil warming experiments at the Harvard Forest (Petersham, Massachusetts, USA) which had experienced 5°C above ambient soil temperatures for 5 and 20 yr at the time of sampling. We assessed fungal diversity and community composition by sequencing the ITS2 region of rDNA using Illumina technology, along with soil C concentrations and chemistry. Three main findings emerged: (1) long‐, but not short‐term warming resulted in compositional shifts in the soil fungal community, particularly in the saprotrophic and unknown components of the community; (2) soil C concentrations and the total C stored in the organic horizon declined in response to both short‐ (5 yr) and long‐term (20 yr) warming; and (3) following long‐term warming, shifts in fungal guild relative abundances were associated with substantial changes in soil organic matter chemistry, particularly the relative abundance of lignin. Taken together, our results suggest that shifts with warming in the relative abundance of fungal functional groups and dominant fungal taxa are related to observed losses in total soil C.
... Climate change can alter the community composition of ECMF by pushing fungi (Kipfer, Egli, Ghazoul, Moser, & Wohlgemuth, 2010) or their host plants (Fernandez et al., 2017) outside their ranges of physiological tolerance (Pickles, Egger, Massicotte, & Green, 2012). ...
... However, most studies to date that have examined ECMF or whole fungal community responses to simulated climate change have found fairly small effects (Fernandez et al., 2017;Mucha et al., 2018;Parrent, Morris, & Vilgalys, 2006;Tu et al., 2015) relative to natural changes in fungal communities observed along large natural gradients of temperature and precipitation (Jarvis, Woodward, Alexander, & Taylor, 2013;Nottingham et al., 2018;Peay et al., 2017;Talbot et al., 2014;Tedersoo et al., 2014). Yet, few datasets currently exist with spatial resolution necessary to make accurate predictions of ECMF response to climate change across relevant geographic regions (Mohan et al., 2014). ...
... Strategies were assigned to the following categories according to Fernandez et al. (2017): contact short (CS), contact medium (CM) and medium long (ML). Because of potential differences in the relationship between DNA copy number and fungal biomass, particularly among functional groups known to differ in their morphology, we restricted our analyses to intraguild comparisons (e.g. ...
Article
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Ectomycorrhizal fungi (ECMF) are partners in a globally distributed tree symbiosis implicated in most major ecosystem functions. However, resilience of ECMF to future climates is uncertain. We forecast these changes over the extent of North American Pinaceae forests. About 68 sites from North American Pinaceae forests ranging from Florida to Ontario in the east and southern California to Alaska in the west. Ectomycorrhizal fungi (Asco‐ and Basidiomycetes). We characterized ECMF communities at each site using molecular methods and modelled climatic drivers of diversity and community composition with general additive, generalized dissimilarity models and Threshold Indicator Taxa ANalysis (TITAN). Next, we projected our models across the extent of North American Pinaceae forests and forecast ECMF responses to climate changes in these forests over the next 50 years. We predict median declines in ECMF species richness as high as 26% in Pinaceae forests throughout a climate zone comprising more than 3.5 million square kilometres of North America (an area twice that of Alaska state). Mitigation of greenhouse gas emissions can reduce these declines, but not prevent them. The existence of multiple diversity optima along climate gradients suggest regionally divergent trajectories for North American ECMF, which is corroborated by corresponding ECMF community thresholds identified in TITAN models. Warming of forests along the boreal–temperate ecotone results in projected ECMF species loss and declines in the relative abundance of long‐distance foraging ECMF species, whereas warming of eastern temperate forests has the opposite effect. Our results reveal potentially unavoidable ECMF species‐losses over the next 50 years, which is likely to have profound (if yet unclear) effects on ECMF‐associated biogeochemical cycles.
... Additional storage or loss of soil C and nutrients over the longer term will be determined by how the biogeochemical cycling activities of soil microorganisms ("effect traits") are linked to traits that allow microbial species to persist under environmental stressors ("response traits") (Allison and Martiny, 2008;Shade et al., 2012;Koide et al., 2014). Both warming and reduced winter snow cover can affect the species composition of soil microbial communities (Lipson and Schmidt, 2004;Allison and Treseder, 2008;Castro et al., 2010;Aanderud et al., 2013;Buckeridge et al., 2013;Luo et al., 2014;DeAngelis et al., 2015;Pold et al., 2015;Fernandez et al., 2016). However, it is unclear how shifts in species abundances under combined growing-season warming and soil freeze/thaw cycles in winter are connected to changes in ecosystem biogeochemistry and especially how species' abilities to cycle C and N through soil is impacted by their tolerance for extreme fluctuations in environmental conditions. ...
... Furthermore, different microbial taxa often have individualistic responses to warming, even within functional groups (Sato et al., 2012;A'Bear et al., 2014a;Tatti et al., 2014;Venugopal et al., 2016). For example, different mycorrhizal fungi can respond positively or negatively to warming, depending on how warming impacts soil moisture, nutrient availability, and the physiology of their host plant (Rillig et al., 2002;Allison and Treseder, 2008;Hawkes et al., 2008;Compant et al., 2010;Fernandez et al., 2016;Wilson et al., 2016;Gange et al., 2018). Similar to warming responses, some microbial taxa can acclimate to freezing conditions, but different species within a trophic group (e.g., ectomycorrhizal fungi, arbuscular mycorrhizal fungi, and free-living saprotrophic decomposers) often differ in the level of tolerance to freezing (Addy et al., 1998;Klironomos et al., 2001;Robinson, 2001). ...
... We found that fungal and bacterial communities in soil responded to climate change manipulations in the field, similar to previous work (Lipson and Schmidt, 2004;Allison and Treseder, 2008;Castro et al., 2010;Aanderud et al., 2013;Buckeridge et al., 2013;Luo et al., 2014;DeAngelis et al., 2015;Pold et al., 2015;Fernandez et al., 2016;Wertz et al., 2016). The microbial taxa that turned over with CCASE treatments represented a small fraction of both bacterial and fungal communities, yet were high in number (Supplementary Figure 2), perhaps because of the high read counts per sample we obtained through sequencing. ...
Article
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Winter air temperatures are rising faster than summer air temperatures in high-latitude forests, increasing the frequency of soil freeze/thaw events in winter. To determine how climate warming and soil freeze/thaw cycles affect soil microbial communities and the ecosystem processes they drive, we leveraged the Climate Change across Seasons Experiment (CCASE) at the Hubbard Brook Experimental Forest in the northeastern United States, where replicate field plots receive one of three climate treatments: warming (+5°C above ambient in the growing season), warming in the growing season + winter freeze/thaw cycles (+5°C above ambient +4 freeze/thaw cycles during winter), and no treatment. Soil samples were taken from plots at six time points throughout the growing season and subjected to amplicon (rDNA) and metagenome sequencing. We found that soil fungal and bacterial community composition were affected by changes in soil temperature, where the taxonomic composition of microbial communities shifted more with the combination of growing-season warming and increased frequency of soil freeze/thaw cycles in winter than with warming alone. Warming increased the relative abundance of brown rot fungi and plant pathogens but decreased that of arbuscular mycorrhizal fungi, all of which recovered under combined growing-season warming and soil freeze/thaw cycles in winter. The abundance of animal parasites increased significantly under combined warming and freeze/thaw cycles. We also found that warming and soil freeze/thaw cycles suppressed bacterial taxa with the genetic potential for carbon (i.e., cellulose) decomposition and soil nitrogen cycling, such as N fixation and the final steps of denitrification. These new soil communities had higher genetic capacity for stress tolerance and lower genetic capacity to grow or reproduce, relative to the communities exposed to warming in the growing season alone. Our observations suggest that initial suppression of biogeochemical cycling with year-round climate change may be linked to the emergence of taxa that trade-off growth for stress tolerance traits.
... However, the impacts of climate change on tree, fungal, and ecosystem health are connected and interdependent, and mycorrhizal fungi can also be directly affected by increasing soil temperatures (Kipfer et al., 2010;Gavito and Azcón-Aguilar, 2012). Higher temperatures can lower a tree's photosynthetic activity, thereby limiting its growth and reducing carbon allocation to its ECM symbionts (Fernandez et al., 2017). Recently, Song et al. (2015) examined fungal partner changes in reaction to heat stress in two tree species, Douglas fir (Pseudotsuga menziesii) and ponderosa pine (Pinus ponderosae), and found that defoliation of the former resulted in stress signaling and resource sharing to the latter. ...
... On the other hand, this ecosystem service depends on the presence of compatible species, and mortality from increasing temperatures simultaneous with heatinduced fungal community shifts, may threaten this resilience. Indeed, Fernandez et al. (2017) reported fungal taxonomic changes as a result of warming temperatures. An increased reliance on Ascomycetes and fungi that provided optimum benefits as photosynthesis capacity decreased was observed (Fernandez et al., 2017). ...
... Indeed, Fernandez et al. (2017) reported fungal taxonomic changes as a result of warming temperatures. An increased reliance on Ascomycetes and fungi that provided optimum benefits as photosynthesis capacity decreased was observed (Fernandez et al., 2017). ...
Article
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Global climate changes have serious consequences on natural ecosystems and cause diverse environmental abiotic stressors that negatively affect plant growth and development. Trees are dependent on their symbiosis with mycorrhizal fungi, as the hyphal network significantly improves the uptake of water and essential mineral nutrients by colonized roots. A number of recent studies has enhanced our knowledge on the functions of mycorrhizal associations between fungi and plant roots. Moreover, a series of timely studies have investigated the impact and benefit of root symbioses on the adaptation of plants to climate change-associated stressors. Trees in temperate and boreal forests are increasingly exposed to adverse environmental conditions, thus affecting their durable growth. In this mini-review, we focus our attention on the role mycorrhizal symbioses play in attenuating abiotic stressors imposed on trees facing climatic changes, such as high temperatures, drought, salinity, and flooding.
... In addition to a sharp decline in the abundance of EMF in the combined heat and drought treatment, EMF diversity dropped by more than 75% relative to the ambient control. Previous studies have documented that EMF diversity declines with drought (Karst et al., 2014;Mohan et al., 2014) while studies of warming temperatures have again focused largely on arctic or boreal systems where results have been mixed (Mohan et al., 2014;Fernandez et al., 2017). In pinyon pine, long-term drought resulted in reduced EMF diversity (Sthultz et al., 2009b;Gehring et al., 2014). ...
... Restoring moister conditions to pinyon pines in the same study area with experimental watering during drought did not increase EMF diversity, suggesting that reductions in diversity with drought may be long term (Patterson et al., 2018). While warming experiments (Fernandez et al., 2017) and drought Karst et al., 2014) appear to favor members of the Ascomycota, their dominance did not differ among treatments in our study. In fact, one of the more drought tolerant species of fungi, the ascomycete, Cenococcum geophilum (Pigott, 1982;Jany et al., 2003), was common (average 31% relative abundance) in the control, heat and drought treatments, but absent from the combined heat and drought treatment (Figure 2). ...
... contributing to their success in these challenging environments are unknown. Studies in cooler, wetter ecosystems, have reported that warming increased EMF taxa with presumably less energetically expensive short distance hyphal exploration types (Fernandez et al., 2017), but EMF taxa with short exploration types dominated in all treatments in our study, consistent with previous studies of P. edulis (Patterson et al., 2018). ...
Article
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Changing climates can cause shifts in temperature and precipitation, resulting in warming and drought in some regions. Although each of these factors has been shown to detrimentally affect forest ecosystems worldwide, information on the impacts of the combined effects of warming and drought is lacking. Forest trees rely on mutualistic root-associated fungi that contribute significantly to plant health and protection against climate stresses. We used a six-year, ecosystem-scale temperature and precipitation manipulation experiment targeted to simulate the climate in 2100 in the Southwestern United States to quantify the effects of drought, warming and combined drought and warming on the root colonization (abundance), species composition and diversity of ectomycorrhizal fungi (EMF), and dark septate fungal endophytes in a widespread woodland tree, pinyon pine (Pinus edulis E.). Our results show that pinyon shoot growth after 6 years of these treatments was reduced more by drought than warming. The combined drought and warming treatment reduced the abundance and diversity of EMF more than either treatment alone. Individual ectomycorrhizal fungal taxa, including the drought tolerant Cenococcum geophilum, were present in all treatments but the combined drought and warming treatment. The combined drought and warming treatment also reduced the abundance of dark septate endophytes (DSE), but did not affect their diversity or species composition. The current year shoot growth of the trees correlated positively with ectomycorrhizal fungal diversity, highlighting the importance of diversity in mutualistic relationships to plant growth. Our results suggest that EMF may be more important than DSE to aboveground growth in P. edulis, but also more susceptible to the negative effects of combined climate stressors.
... Fungal taxonomic and functional diversity in high-latitude ecosystems are strongly influenced by temperature Asemaninejad et al., 2018;Bennett & Classen, 2020;Salazar et al., 2020;Treseder et al., 2016). For example, experimental warming may stimulate ECM mycelial production (Leppälammi-Kujansuu et al., 2013) and impact the abundance of ECM exploration types with differing mycelial morphology, nutrient uptake strategies, and enzymatic degradation abilities (Deslippe et al., 2011;Fernandez et al., 2017;Morgado et al., 2015;Mucha et al., 2018). However, warming effects on mycelial morphology may strongly depend upon the performance of ECM plant hosts (Clemmensen et al., 2015;Fernandez et al., 2017), often via interactions with other edaphic and environmental factors including soil moisture and nitrogen mineralization. ...
... For example, experimental warming may stimulate ECM mycelial production (Leppälammi-Kujansuu et al., 2013) and impact the abundance of ECM exploration types with differing mycelial morphology, nutrient uptake strategies, and enzymatic degradation abilities (Deslippe et al., 2011;Fernandez et al., 2017;Morgado et al., 2015;Mucha et al., 2018). However, warming effects on mycelial morphology may strongly depend upon the performance of ECM plant hosts (Clemmensen et al., 2015;Fernandez et al., 2017), often via interactions with other edaphic and environmental factors including soil moisture and nitrogen mineralization. ...
... Observed differences in mycelial morphology between the two ends of the temperature gradient at SPRUCE may be related to ECM host performance (Fernandez et al., 2017). At SPRUCE, multiple data streams indicate that L. laricina individuals may be better acclimating to warming than P. mariana individuals (Dusenge et al., 2020;Peters et al., unpublished (Clemmensen et al., 2015). ...
Article
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Mycorrhizal fungi enable plants to thrive in the cold, waterlogged, organic soils of boreal peatlands and, with saprotrophic fungi, largely contribute to the sequestration of atmospheric carbon in peat. Hence, fungi support the contribution of peatlands to global climate regulation, on which society depends. Here, we used high‐resolution minirhizotrons for an unprecedented glimpse of the belowground world of a forested bog and highlighted linkages between environmental change and the abundance, dynamics, and morphology of vascular plant fine roots and fungal mycelium. These changes may have implications for peat carbon accumulation on the boreal landscape. Mycorrhizal fungi enable plants to thrive in the cold, waterlogged, organic soils of boreal peatlands and, with saprotrophic fungi, largely contribute to the sequestration of atmospheric carbon in peat. Hence, fungi support the contribution of peatlands to global climate regulation, on which society depends. Here we used high‐resolution minirhizotrons for an unprecedented glimpse of the belowground world of a forested bog and highlighted linkages between environmental change and the abundance, dynamics, and morphology of vascular plant fine roots and fungal mycelium. These changes may have implications for peat carbon accumulation on the boreal landscape. Summary Minirhizotron technology has rarely been deployed in peatlands which has limited our understanding of root‐fungal dynamics in one of planet's most carbon‐dense ecosystems. We used novel, high‐resolution minirhizotrons in a forested bog to explore temporal variation in the abundance and growth of plant fine roots and fungal mycelium with changes in peat temperature and moisture. We utilized the framework of the Spruce and Peatland Responses Under Changing Environments experiment and focused on two minirhizotron tubes installed at the coldest (+0, elevated CO2) and warmest (+9°C, elevated CO2) ends of the experimental temperature gradient, respectively. We found that in warmer and drier peat, ericaceous shrub roots and ectomycorrhizal fungal rhizomorphs were more abundant, and the growth of rhizomorphs and sporocarps was greater. In turn, fine roots of trees, ectomycorrhizas, and dark‐colored fungal hyphae were more abundant in colder, wetter peat. Ultimately, the belowground active season for both plant roots and fungi was extended by 62 days at the warmest compared to the coldest end of the gradient, with implications for belowground carbon, water, and nutrient fluxes. High‐resolution minirhizotrons in peatlands provided an unprecedented view of ericaceous shrub and tree fine roots and their mycorrhizal fungal partners in situ. Therefore, this technology advanced our understanding of linkages between environmental change and the abundance, morphology, and dynamics of vascular plant fine roots and fungal mycelium.
... Numerous observational and experimental studies have reported that most plants exhibit higher intensities of mycorrhizal colonization when exposed to rising temperatures (Rillig et al. 2002a, Büscher et al. 2012, Vega-Frutis et al. 2014, likely because warming accelerate the metabolism of plants and allow them to translocate a higher amount of photosynthates to the fungi (Kytoviita and Ruotsalainen 2007). Conversely, drought seems to compromise this plant-microorganism symbiosis, likely because water limitation usually decreases carbon assimilation and availability for allocation to mycorrhizal fungi in stressed host-plants (Augé 2001, Fernández et al. 2017. However, this is not a universal pattern; previous studies have reported opposite climate-induced responses to the above-mentioned common trends, with negative effects of warming or stimulating effects of drought on root colonization rates by mycorrhizal fungi (reviewed by Compant et al. 2010, Mohan et al. 2014). ...
... The enhanced activity induced by warming could be explained by the increased metabolism that both plants and fungi usually exhibit under warmer conditions, which can result in higher rates of nutrient transfer from the fungi to the plant as well as higher C allocation from the plant to the fungi (Hawkes et al. 2008). The reduced AMF in response to rising temperatures contrasts with the positive effects of warming reported by numerous studies (reviewed by Compant et al. 2010, Mohan et al. 2014, but is in line with the results shown by other works in ecosystems where productivity is mainly limited by water availability (Fernández et al. 2017, León-Sánchez et al. 2018. These authors attribute the negative impact of warming on mycorrhizal abundance to the detrimental effects caused by heat stress on the plant during late spring and summer, potentially decreasing its net photosynthetic rate and leading to large reductions in photosynthate availability for allocation to mycorrhizal fungi. ...
Article
Mycorrhizal fungi are key components of whole-plant adaptive strategies to cope with different abiotic and biotic constraints. Although they are particularly sensitive to different global change drivers, there are still many gaps on the mechanisms underpinning shifts in mycorrhizal associations under different climatic and management scenarios. We carried out a field manipulative experiment of rainfall exclusion and increased temperature aimed to evaluate the impact of forecasted warming and drying on mycorrhizal associations of savanna plant communities subjected to different grazing history. Additionally, we compiled detailed information on the abiotic and biotic environment with the final aim of disentangling the direct and indirect effects of climate change on this widespread mycorrhizal symbiosis. Our results suggest that climate change could induce relevant changes in mycorrhizal associations, primarily promoted by warming, which decreased the abundance of mycorrhizae but induced higher activity of nutrient exchange between the host–plant and the mycosymbiont. Temperature did not only affect this symbiosis in a direct way, but also exerted relevant indirect effects via changes in soil functioning and other root-colonizing microorganisms such as dark septate endophytes. Grazing history influenced the allocation of fungal structures inside the host-root, but its effect differed as a function of the climatic treatment. Results from this study suggest that mycorrhizal fungi might become less prevalent in plant communities inhabiting savanna ecosystems under future scenarios of increasing aridity. In agreement with this finding, higher temperatures also promoted the predominance of plants with root traits that favour efficient resource acquisition by themselves without the help of a mycorrhizal partner. Our results provide new insights into the interactive effects of the two main threats facing Mediterranean savanna ecosystems, as well as potentially useful information to be applied in ecologically-based management strategies aimed at attenuating the potential impact of global change on mycorrhizal fungi.
... [4] ,在生态系统碳(C)、氮(N)循环过程扮演着重要角色。据估计地球上大约 90%的陆生植物具有菌 根共生体 [5] ,可利用约 2.5%-20.0%的植物光合作用所同化的 C 来构建和维持外延菌丝 [6] ,在地下形成庞大 的菌丝网络直接或间接地与其他生物相互作用并影响整个生态系统物质循环过程。如,光合产的物固定与 分配 [6][7] ,养分元素的吸收 [4] ,有机质的分解 [8] 等。已有研究发现菌根真菌生物量及菌丝周转是土壤重要的 C 汇来源 [9] ,约占土壤微生物总量的 30% [10] ,并驱动 N 在菌丝网络系统内传输,有效调节生态系统内植物 间 N 的再分配 [4,11] 。同时,菌根还可以通过分泌胞外酶直接或间接参与凋落物酶降解过程。如,磷酸酶、 几丁质酶和海藻糖酶等土壤酶水平的提高,可促进有机质中复杂有机 C、N、磷(P)的降解 [12] 。因此,菌 根已经成为土壤 C、N 循环研究中不可或缺的重要部分 外生菌根(Ectomycorrhizae, ECM)作为菌根的重要类型之一,是北方高山/亚高山森林生态系统进程 中最活跃的驱动力之一 [13] ,同时也是影响植物对全球变化响应的重要因素。随着全球变暖的不断加剧,外 生菌根及其介导土壤 C、N 过程对增温的响应对于预测气候变暖背景下生态系统物质循环至关重要。温度 升高可以影响土壤菌根真菌多样性和群落结构、改变植物生长及生理特性 [13][14] 。因此,气候变暖势必会影 响菌根所介导的地下生态学过程。目前,在气候变化下菌根的研究主要集中在根系的侵染状况及菌根真菌 群落组成、多样性等方面 [14][15] 。而关于在菌根介导的土壤 C、N 过程对增温响应方面的报道较少。并且, 由于菌根共生的复杂性、区域异质性以及研究手段的多样性等方面的原因,气候变暖对菌根介导下的土壤 C、N 过程的研究结果并不一致 [16][17][18][19] 。例如,常越 [16] 研究证明增温会显著降低菌根真菌介导的土壤硝态氮 和铵态氮含量,但增加了总碳含量;然而,Fernandez 等 [17] 研究却表明,当高于环境温度 3.4 ℃时,外生菌 根介导的土壤有效氮呈上升趋势。Clemmensen [18] 等的研究表明增温将促进外生菌根真菌介导的 C、N 循环, 增加北极苔原土壤有机质的积累。 Rillig [19] [24] 。小区内按 20 cm × 30 cm 植株距离栽植 5 年 生粗枝云杉幼苗。参考 Heinemeyer [25] and C under warming (P < 0.05);  indicating significant differences between warming and control (*, P < 0.05; **, P < 0.01; ***, P < 0.001). W: warming, G: growth tubes type, and W * G: interaction of warming and growth tubes type. ...
... [4] ,在生态系统碳(C)、氮(N)循环过程扮演着重要角色。据估计地球上大约 90%的陆生植物具有菌 根共生体 [5] ,可利用约 2.5%-20.0%的植物光合作用所同化的 C 来构建和维持外延菌丝 [6] ,在地下形成庞大 的菌丝网络直接或间接地与其他生物相互作用并影响整个生态系统物质循环过程。如,光合产的物固定与 分配 [6][7] ,养分元素的吸收 [4] ,有机质的分解 [8] 等。已有研究发现菌根真菌生物量及菌丝周转是土壤重要的 C 汇来源 [9] ,约占土壤微生物总量的 30% [10] ,并驱动 N 在菌丝网络系统内传输,有效调节生态系统内植物 间 N 的再分配 [4,11] 。同时,菌根还可以通过分泌胞外酶直接或间接参与凋落物酶降解过程。如,磷酸酶、 几丁质酶和海藻糖酶等土壤酶水平的提高,可促进有机质中复杂有机 C、N、磷(P)的降解 [12] 。因此,菌 根已经成为土壤 C、N 循环研究中不可或缺的重要部分 外生菌根(Ectomycorrhizae, ECM)作为菌根的重要类型之一,是北方高山/亚高山森林生态系统进程 中最活跃的驱动力之一 [13] ,同时也是影响植物对全球变化响应的重要因素。随着全球变暖的不断加剧,外 生菌根及其介导土壤 C、N 过程对增温的响应对于预测气候变暖背景下生态系统物质循环至关重要。温度 升高可以影响土壤菌根真菌多样性和群落结构、改变植物生长及生理特性 [13][14] 。因此,气候变暖势必会影 响菌根所介导的地下生态学过程。目前,在气候变化下菌根的研究主要集中在根系的侵染状况及菌根真菌 群落组成、多样性等方面 [14][15] 。而关于在菌根介导的土壤 C、N 过程对增温响应方面的报道较少。并且, 由于菌根共生的复杂性、区域异质性以及研究手段的多样性等方面的原因,气候变暖对菌根介导下的土壤 C、N 过程的研究结果并不一致 [16][17][18][19] 。例如,常越 [16] 研究证明增温会显著降低菌根真菌介导的土壤硝态氮 和铵态氮含量,但增加了总碳含量;然而,Fernandez 等 [17] 研究却表明,当高于环境温度 3.4 ℃时,外生菌 根介导的土壤有效氮呈上升趋势。Clemmensen [18] 等的研究表明增温将促进外生菌根真菌介导的 C、N 循环, 增加北极苔原土壤有机质的积累。 Rillig [19] [24] 。小区内按 20 cm × 30 cm 植株距离栽植 5 年 生粗枝云杉幼苗。参考 Heinemeyer [25] and C under warming (P < 0.05);  indicating significant differences between warming and control (*, P < 0.05; **, P < 0.01; ***, P < 0.001). W: warming, G: growth tubes type, and W * G: interaction of warming and growth tubes type. ...
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开展川西亚高山建群种云杉(Picea asperata)外生菌根及外延菌丝土壤碳(C)和氮(N)过程对 增温响应的研究,对于未来气候变化背景下区分及估算菌根与外延菌丝对亚高山针叶林生态系统 C、N 循 环过程的影响具有重要意义。采用红外辐射加热器模拟气候变暖,同时采用不同孔径生长管区分根系(菌 根) (R 管)、外延菌丝(H 管)和无根无菌丝土壤(C 管),研究 3 种土壤理化性质、土壤有机碳(SOC)、 微生物量及土壤 C、N 转化过程关键土壤酶活性对增温的响应。结果表明,增温显著降低了 3 种生长管土 壤含水量、硝态氮(NO3-N)与铵态氮(NH4 +-N)的含量(P < 0.05),显著提高了 β-D-葡萄糖苷酶(BG) (C 管除外)及 N-乙酰葡萄糖苷酶(NAG)的活性(P < 0.05),而对土壤 pH、土壤有机碳、微生物量碳 (MBC)、外生菌根真菌(ECMf)生物量均无显著影响(P > 0.05)。无论增温与否,SOC 含量与 BG、 NAG 酶活性在 R 管与 H 管中均无显著差异,但 R 管与 H 管中土壤 NO3-N、NH4 +-N、SOC 含量,ECMf 生物量及 BG、NAG 酶活性均显著高于 C 管。此外,增温后 H 管土壤 NO3-N、NH4 +-N 含量及 ECMf 生物 量,分别由 R 管的 66%、82.1%及 74.1%,上升为 95.4%、98.2%以及 94.2%,二者之间的差异明显缩小。 结果说明,外生菌根作为川西亚高山针叶林主要建群种云杉根系的重要组成部分,其外延菌丝对土壤 C、N 过程,尤其是土壤 C 库及关键酶活性,具有几乎与根同等重要影响,而未来气候变暖背景下外延菌丝的作 用将更为明显。
... Taxonomic diversity analyses were carried out in R 4.0.3 (R Core Development Team 2008) using custom scripts and the phyloseq, vegan, metacoder and ggplot2 packages [32][33][34][35] According to Fernandez et al. (2017) [36], we transformed read counts into relative abundances by averaging the number of reads per sample, multiplied by 10,000 and transformed to the next integer to be used as counts. Species richness (observed richness and Shannon index) between organs (root or stem) and conditions (symptomatic, asymptomatic, feral) were tested using non-parametric Kruskal-Wallis and pairwise Wilcoxon rank sum tests. ...
... Taxonomic diversity analyses were carried out in R 4.0.3 (R Core Development Team 2008) using custom scripts and the phyloseq, vegan, metacoder and ggplot2 packages [32][33][34][35] According to Fernandez et al. (2017) [36], we transformed read counts into relative abundances by averaging the number of reads per sample, multiplied by 10,000 and transformed to the next integer to be used as counts. Species richness (observed richness and Shannon index) between organs (root or stem) and conditions (symptomatic, asymptomatic, feral) were tested using non-parametric Kruskal-Wallis and pairwise Wilcoxon rank sum tests. ...
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The worldwide production of vanilla, a native orchid from Mexico, is greatly affected by stem and root rot disease (SRD), typically associated with Fusarium oxysporum fungi. We hypothesized that the presence of Fusarium species in vanilla is not sufficient for the plant to express symptoms of the disease. We described the taxonomic composition of endophytic microbiomes in symptomatic and asymptomatic vanilla plants using 16S and ITS rDNA metabarcoding, and ITS Sanger sequences generated from fungal isolates. We compared the bacterial and fungal diversity in vanilla plants from a long-term plantation, and from feral plants found near abandoned plantations that did not present SRD symptoms. No significant differences were found in the species richness of the bacterial and fungal microbiome among feral, or asymptomatic and symptomatic cultivated vanilla. However, significant differences were detected in both fungal and bacterial diversity from different organs in the same plant, with roots being more diverse than stems. We found that Proteobacteria and Actinobacteria, as well as the fungal families Nectriaceae and Xylariaceae, constitute the core of the vanilla microbiome that inhabits the root and stem of both cultivated and feral plants. Our work provides information on the microbial diversity associated to root and stem rot in vanilla and lays the groundwork for a better understanding of the role of the microbiome in vanilla fungal diseases.
... ECM communities are affected by soil temperaturefor example, warming led to an increase in the biomass of Cenococcum spp. (Fernandez et al., 2017) and nematode communities may also be indirectly influenced by the extent of extramatrical hyphae of ECM fungi. Trophic structure of soil nematodes in cool to temperate pine forests has been characterized by the predominance of both bacterivorous and fungivorous nematodes (Háněl, 2001;Zhang et al., 2015;Kitagami et al., 2017Kitagami et al., , 2018, and those two trophic groups of nematodes play fundamental roles in nutrient cycling in the forests. ...
... Moreover, the warming effects led to a change in ECM fungal communities, such as an increase in the biomass of Cenococcum spp. (Fernandez et al., 2017). In our study, temperature and pine seedlings synergistically increased the density of fungivorous nematodes, which, in turn, might be consumed by omnivorous ones. ...
Article
Nematodes serve a key role in soil nutrient cycling by eating bacterial cells and fungal hyphae. However, little is known about how temperature changes affect multi-trophic interactions among host trees, root-associating fungi, and nematodes. The aim of this study was to identify abiotic and/or biotic factors that affect soil nematode communities. We constructed a pot microcosm with sandy soils from a coastal Pinus thunbergii forest. The soil-filled pots were incubated for 8 months at 20, 25, or 30 °C with or without pine seedlings. In the pots with seedlings, we measured the percentages of black, white, and brown ectomycorrhizal (ECM) formations on roots. Nematodes retrieved from the soils were morphologically identified to genus and differentiated by both trophic and community structures. The occurrence of ECM formation ranged from 85.7%–91.9%. Black ECM roots were significantly dominant at 30 °C (47.0 %), whereas white ones were significantly dominant at 20 °C (43.0 %) and 25 °C (53.0 %). The number of nematodes at 25 and 30 °C was significantly greater than that at 20 °C irrespective of the presence or absence of seedlings. In terms of trophic compositions, the relative abundance of fungivorous nematodes significantly increased from 10.4 % at 20 °C to 27.5 % at 25 °C to 44.6 % at 30 °C in the presence of pine seedlings. A non-metric multidimensional scaling scatter plot showed that the nematode communities clustered significantly among temperature treatments. Structural equation modeling indicated that nematode trophic compositions were directly regulated by temperature and the presence of pine seedlings. Our findings suggest that temperature has some cascading effects on the formation of nematode communities, and pine seedlings and associating ECM fungi contributed synergistically to the formation of their communities.
... They harbor hyperdiverse fungal communities that act as key decomposers (Schneider et al., 2012;Peay et al., 2016) and, in turn, are regulators of forest soil C storage (Averill and Hawkes, 2016;Frey, 2019;Lindahl et al., 2021). Increasing evidence shows that fungal communities are sensitive to environmental changes, including anthropogenic nitrogen (N) deposition (Lilleskov et al., 2011;Morrison et al., 2016;Van der Linde et al., 2018;Moore et al., 2021), climate warming (Treseder et al., 2016;Fernandez et al., 2017;Morrison et al., 2019;Cao et al., 2020), nonnative invasive species (Lekberg et al., 2013;Gibbons et al., 2017;Anthony et al., 2019), and myriad other global changes (see review by Zhou et al., 2020). How fungi respond to global changes at the local level can have cascading effects throughout forests, influencing tree growth and mortality and soil carbon storage. ...
... Climate warming and atmospheric N deposition are particularly important environmental factors that can influence soil fungi, SOM cycling, and soil C storage. Warming often decreases fungal biomass Morrison et al., 2019) and has been shown to shift fungal community structure (Morrison et al., 2019;Cao et al., 2020) and the relative abundances of key fungal taxa (Fernandez et al., 2017;Mucha et al., 2018). Warming can also alter SOM chemistry by accelerating decomposition, resulting in lower soil C storage (Pisani et al., 2015;Melillo et al., 2017). ...
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Soil fungi are key regulators of forest carbon cycling and their responses to global change have effects that ripple throughout ecosystems. Global changes are expected to push many fungi beyond their environmental niches, but there are relatively few studies involving multiple, simultaneous global change factors. Here, we studied soil fungal diversity, community composition, co-occurrence patterns, and decomposition gene responses to 10 years of soil warming and nitrogen addition, alone and in combination. We specifically examined whether there were fungal community characteristics that could explain changes in soil carbon storage and organic matter chemistry in chronically warmed and fertilized soil. We found that fungal communities in warmed soils are less diverse and shift in composition. Warming also favored hyperdominance by a few mycorrhizal fungal species and lowered manganese peroxidase but increased hydrolytic enzyme encoding gene potentials. Nitrogen addition did not significantly affect fungal community composition but, like warming, did reduce fungal diversity and favored overdominance by a unique set of mycorrhizal taxa. Warming alone and in combination with nitrogen addition also reduced negative but increased positive fungal co-occurrence probabilities, promoting species coexistence. Negative fungal co-occurrence was positively correlated to soil carbon content, while the proportion of fungal hydrolytic enzyme encoding genes was negatively correlated with soil carbon content. This may reflect fungal life history trade-offs between competition (e.g., reduced negative co-occurrence) and resource acquisition (e.g., higher abundance of hydrolytic enzyme encoding genes) with implications for carbon storage.
... How fungi respond to invasion can also feed-back to impact native plant communities (Stinson et al. 2006), soil carbon (C) storage (Ehrenfeld 2003;Tamura and Tharayil 2014), and ecosystem restoration efforts (Lankau et al. 2014;Anthony et al. 2019). Fungi are highly sensitive to abiotic stressors such as warming and nitrogen deposition (Lilleskov et al. 2011;Geml et al. 2015;Morrison et al. 2016;Fernandez et al. 2017), but the interactive effects of invasion and concurrent abiotic global changes on soil fungi are rarely investigated (Wheeler et al. 2017). ...
... As decomposers, mycorrhizal symbionts, and pathogens, soil fungi strongly shape the functioning of forested ecosystems (Treseder and Lennon 2015). What we know about their sensitivities to global change primarily comes from singlefactor studies (Lekberg et al. 2007;Lilleskov et al. 2011;Morrison et al. 2016;Fernandez et al. 2017;Gibbons et al. 2017), but global change factors typically do not occur in isolation from each other (Aber et al. 2001). The impact of multiple global change stressors on microbial communities are seldom tested-only 20% of studies have examined more than one factor, and only 1% have examined more than two factors (Rillig et al. 2019). ...
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The impacts of invasive species on biodiversity may be mitigated or exacerbated by abiotic environmental changes. Invasive plants can restructure soil fungal communities with important implications for native biodiversity and nutrient cycling, yet fungal responses to invasion may depend on numerous anthropogenic stressors. In this study, we experimentally invaded a long-term soil warming and simulated nitrogen deposition experiment with the widespread invasive plant Alliaria petiolata (garlic mustard) and tested the responses of soil fungal communities to invasion, abiotic factors, and their interaction. We focused on the phytotoxic garlic mustard because it suppresses native mycorrhizae across forests of North America. We found that invasion in combination with warming, but not under ambient conditions or elevated nitrogen, significantly reduced soil fungal biomass and ectomycorrhizal relative abundances and increased relative abundances of general soil saprotrophs and fungal genes encoding for hydrolytic enzymes. These results suggest that warming potentially exacerbates fungal responses to plant invasion. Soils collected from uninvaded and invaded plots across eight forests spanning a 4 °C temperature gradient further demonstrated that the magnitude of fungal responses to invasion was positively correlated with mean annual temperature. Our study is one of the first empirical tests to show that the impacts of invasion on fungal communities depends on additional anthropogenic pressures and were greater in concert with warming than under elevated nitrogen or ambient conditions.
... The findings of this study highlighted that mycelial dynamics of mycorrhizal fungi in Mediterranean forests are likely to be constrained by lack of water (Castaño et al., 2017(Castaño et al., , 2018b. Water limitations may directly restrict mycorrhizal growth by immediate water stress or indirectly via reduced host tree performance (Fernandez et al., 2017), reducing allocation of C to belowground and, thus, limiting the mycorrhizal C availability. Furthermore, water is required for functioning of hydrolytic enzymes of mycorrhizal fungi, and restricted water access is likely to have consequences on nutrient availability by reducing enzymes' capacities to degrade soil organic matter (Sardans & Peñuelas, 2013). ...
... medium-, fringe-and long-distance exploration types) may imply a higher C demand on the host, as more energy would be required to support the maintenance of a large biomass (Rygiewicz & Andersen, 1994), while species forming small mycelial networks (e.g. contact and short-distance exploration types) have been demonstrated to increase in abundance under dry conditions (Fernandez et al., 2017;Castaño et al., 2018b). The extent to which belowground C allocation changes with drought probably relates to belowground C demands that are likely to vary between forests types, because of differences in mycorrhizal community compositions. ...
Article
In forests, ectomycorrhizal mycelium is pivotal for driving soil carbon and nutrient cycles, but how ectomycorrhizal mycelial dynamics vary in ecosystems with drought periods is unknown. We quantified production and turnover of mycorrhizal mycelium in Mediterranean Pinus pinaster, Pinus sylvestris and Quercus ilex forests and related the estimates to standardized precipitation index (SPI), to study how mycelial dynamics relates to tree species and drought‐moisture conditions. Production and turnover of mycelium was estimated between July‐February, by quantifying the fungal biomass (ergosterol) in ingrowth mesh bags and using statistical modelling. SPI for time scales of 1 to 3 months, was calculated from precipitation records and precipitation data over the study period. Forests dominated by Pinus trees displayed higher biomass but were seasonally more variable, as opposed to Q. ilex forests where the mycelial biomass remained lower and stable over the season. Production and turnover respectively varied between 1.4‐5.9 kg ha‐1 day‐1 and 7.2‐9.9 times year‐1 over the different forest types and were positively correlated with 2‐ and 3‐month SPI over the study period. Our results demonstrate that mycorrhizal mycelial biomass vary with season and tree species and we speculate that production and turnover are related to physiology and plant‐host performance during drought.
... Similar to others studies(Fernandez et al., 2017;Mucha et al., 2018;Parts et al., 2019), soil warming did not affect EcM fungal diversity.Fernandez et al. (2017) attributed the lack of a significant effect of experimental warming on fungal diversity to the high density of boreal and temperate host species in their experimental site, whileMucha et al. (2018) highlighted the dominance of generalist EcM species in their study. However, an increase in EcM fungal diversity with warming was reported in the arctic(Deslippe et al., 2011) and ...
... Similar to others studies(Fernandez et al., 2017;Mucha et al., 2018;Parts et al., 2019), soil warming did not affect EcM fungal diversity.Fernandez et al. (2017) attributed the lack of a significant effect of experimental warming on fungal diversity to the high density of boreal and temperate host species in their experimental site, whileMucha et al. (2018) highlighted the dominance of generalist EcM species in their study. However, an increase in EcM fungal diversity with warming was reported i ...
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Climate warming is predicted to affect temperate forests severely, but the response of fine roots, key to plant nutrition, water uptake, soil carbon and nutrient cycling is unclear. Understanding how fine roots will respond to increasing temperature is a prerequisite for predicting the functioning of forests in a warmer climate. We studied the response of fine roots and their ectomycorrhizal (EcM) fungal and root‐associated bacterial communities to soil warming by 4 °C in a mixed spruce‐beech forest in the Austrian Limestone Alps after 8 and 14 years of soil warming, respectively. Fine root biomass (FRB) and fine root production were 17% and 128% higher in the warmed plots, respectively, after 14 years. The increase in FRB (13%) was not significant after 8 years of treatment, whereas specific root length, specific root area, and root tip density were significantly higher in warmed plots at both sampling occasions. Soil warming did not affect EcM exploration types and diversity, but changed their community composition, with an increase in the relative abundance of Cenoccocum at 0 – 10 cm soil depth, a drought‐stress tolerant genus, and an increase in short and long‐distance exploration types like Sebacina and Boletus at 10 – 20 cm soil depth. Warming increased the root‐associated bacterial diversity but did not affect their community composition. Soil warming did not affect nutrient concentrations of fine roots, though we found indications of limited soil phosphorus (P) and potassium (K) availability. Our findings suggest that, in the studied ecosystem, global warming could persistently increase soil carbon inputs due to accelerated fine root growth and turnover, and could simultaneously alter fine root morphology and EcM fungal community composition towards improved nutrient foraging.
... Warming in high-latitude biomes is projected to decrease snowpack in winter, causing soils to freeze more frequently . These dual soil temperature shifts -warming during the growing season and increased frequency of freeze/thaw cycles in winter -can shift soil microbial communities, as well as their growth rates and C-cycling enzyme activities, either separately (Lipson and Schmidt, 2004;Allison and Treseder, 2008;Aanderud et al., 2013;Buckeridge et al., 2013;Luo et al., 2014;DeAngelis et al., 2015;Pold et al., 2015;Fernandez et al., 2016), or in combination Garcia et al., 2020). However, it is still unclear why such shifts occur. ...
... By contrast, selection for taxa that generate high oxidase activity (which targets more recalcitrant C molecules, e.g., lignin)can occur after longer-term (>20 years) warming conditions deplete labile C pools in soil Chen et al., 2018Chen et al., , 2020. Because fungal species differ in their intrinsic ability to adjust morphology, behavior, or physiological states based on environmental conditions (Westeberhard, 1989), the ability of some species (and not others) to acclimate to new temperaturesespecially in terms of their labile C (e.g., cellulose) use or their carbon use efficiency-may account for shifts in fungal community composition observed with experimental warming Luo et al., 2014;DeAngelis et al., 2015;Pold et al., 2015;Fernandez et al., 2016). Alternatively, some fungal taxa may evolve in response to elevated temperatures on relatively short timescales-as short as a few weeks or months in some cases-aided by their relatively short generation times (Leu and Murray, 2006;Bradford et al., 2008;Dettman et al., 2008;Romero-Olivares et al., 2015). ...
Article
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Projections for the northeastern United States indicate that mean air temperatures will rise and snowfall will become less frequent, causing more frequent soil freezing. To test fungal responses to these combined chronic and extreme soil temperature changes, we conducted a laboratory-based common garden experiment with soil fungi that had been subjected to different combinations of growing season soil warming, winter soil freeze/thaw cycles, and ambient conditions for 4 years in the field. We found that fungi originating from field plots experiencing a combination of growing season warming and winter freeze/thaw cycles had inherently lower activity of acid phosphatase, but higher cellulase activity, that could not be reversed in the lab. In addition, fungi quickly adjusted their physiology to freeze/thaw cycles in the laboratory, reducing growth rate, and potentially reducing their carbon use efficiency. Our findings suggest that less than 4 years of new soil temperature conditions in the field can lead to physiological shifts by some soil fungi, as well as irreversible loss or acquisition of extracellular enzyme activity traits by other fungi. These findings could explain field observations of shifting soil carbon and nutrient cycling under simulated climate change.
... Mycorrhizal fungal species also vary in extra-radical hyphal (ERH) density (Jakobsen et al. 1992, Duan et al. 2011) and turnover (reviewed in Chagnon et al. 2013) all of which may be related to species and genotype level variation in hyphal fusion rates (Pepe et al. 2016). These traits, and others, are responsive to climatic change (Fernandez et al. 2017). For example, mycorrhizal fungi also vary in melanin content (Wright et al. 1996), and increases in mycorrhizal fungal melanin have been linked to variation in water availability (Deveautour et al. 2019). ...
... Warming can promote both EcM and growth of EcM associated plants in the field (Deslippe et al. 2011). Warming can also influence host plant associations in ways that alter mycorrhizal fungal communities, and these host driven shifts in mycorrhizal fungi, coupled with changes in soil nutrient availability, could lead to significant changes in host plant success especially at the warm edges of plant ranges (Fernandez et al. 2017). ...
Article
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Climate change is altering the interactions among plants and soil organisms in ways that will alter the structure and function of ecosystems. We reviewed the literature and developed a map of studies focused on how the three most common types of mycorrhizal fungi (arbuscular mycorrhizal (AM), ectomycorrhizal (EcM), and ericoid mycorrhizal (ErM) fungi) respond to elevated atmospheric carbon dioxide concentrations (eCO2), climatic warming, and changes in the distribution of precipitation. Broadly, we ask how do mycorrhizal fungi respond to climate change, how do these responses vary by fungal type, and how do mycorrhizal traits influence plant adaptation, movement, or extinction in response to climatic change? First, we found that 92% of studies were conducted in the northern hemisphere, and plant host, ecosystem type and study location were only correlated with each other in the northern hemisphere because studies across all mycorrhizal fungal types were only common in the northern hemisphere. Second, we show that temperature and rainfall variability had more variable effects than eCO2 on mycorrhizal fungal structures, but these effects were context dependent. Third, while mycorrhizal fungal types vary in their responses to climate change, it appears that warming lead to more variable responses in ectomycorrhizal than in arbuscular mycorrhizal fungi. Finally, we discuss common traits of mycorrhizal fungi that could aid in fungal and plant adaption to climate change. We posit that mycorrhizal fungi can buffer plant hosts against extinction risk, they can facilitate or retard the dispersal success of plants moving away from poor environments, and, by buffering host plants, they can enable host plant adaptation to new climates. All of these influences are, however, context dependent a finding that reflects the complex traits of mycorrhizal fungi as a group, the diversity of plant species they associate with and the variation in ecosystems in which they reside. Overall, while we point out many gaps in our understanding of the influence of climate changes on mycorrhizal fungi, we also highlight the large number of opportunities for researching plant and mycorrhizal fungal responses to and mitigation of climate changes.
... Moreover, despite the high EM taxonomic diversity in the Alps, there was a high degree of functional redundancy with similar traits shared by many different fungi; we found EM fungal communities dominated by short-distance explorers. In forest ecosystems, short explorers thrive at higher soil nutrient availability (Lilleskov et al., 2011;Jarvis et al., 2013), in colder climates, where hosts have lower photosynthetic capacity (Fernandez et al., 2017), or in colder and drier environments (Castaño et al., 2018;Botnen et al., 2019;Defrenne et al., 2019). Alpine EM plants are adapted to harsh conditions, at least partly through a reliance on shortdistance or contact explorers (Fig. 3a). ...
... Moreover, despite the high EM taxonomic diversity in the Alps, there was a high degree of functional redundancy with similar traits shared by many different fungi; we found EM fungal communities dominated by short-distance explorers. In forest ecosystems, short explorers thrive at higher soil nutrient availability (Lilleskov et al., 2011;Jarvis et al., 2013), in colder climates, where hosts have lower photosynthetic capacity (Fernandez et al., 2017), or in colder and drier environments (Castaño et al., 2018;Botnen et al., 2019;Defrenne et al., 2019). Alpine EM plants are adapted to harsh conditions, at least partly through a reliance on shortdistance or contact explorers (Fig. 3a). ...
Article
Alpine habitats are one of the most vulnerable ecosystems to environmental change, however, little is known about the drivers of plant‐fungal interactions in these ecosystems and their resilience to climate change. We investigate the influence of the main drivers of ectomycorrhizal (EM) fungal communities along elevation and environmental gradients in the alpine zone of the European Alps and measured their degree of specialization using network analysis. We sampled ectomycorrhizas of Dryas octopetala, Bistorta vivipara and Salix herbacea, and soil fungal communities at 28 locations across five countries, from the treeline to the nival zone. We found that: i) EM fungal community composition, but not richness, changes along elevation, ii) there is no strong evidence of host specialization, however, EM fungal networks in the alpine zone and within these, EM fungi associated with snowbed communities, are more specialized than in other alpine habitats, iii) plant host population structure does not influence EM fungal communities, and iv) most variability in EM fungal communities is explained by fine‐scale changes in edaphic properties, like soil pH and total nitrogen. The higher specialization and narrower ecological niches of these plant‐fungal interactions in snowbed habitats make these habitats particularly vulnerable to environmental change in alpine ecosystems.
... This may also explain the higher Imleria badia occurrence. Furthermore, Clemmensen [107], Morgado [108], and Fernandez [109] classify the Bay Bolete to the group of long-distance exploration fungi. In other words, this species is able to create long rhizomorphs that enable efficient habitat penetration. ...
Article
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Background: Scientists frequently raise the topic of data deficiency related to the abundance and distribution of macrofungi in the context of climate change. Our study is the first detailed documentation on locals' perception of fungal ecology which covers a large mycophilous region of Europe (Mazovia, Poland). Methods: A total of 695 semi-structured interviews were carried out among local informants in 38 localities proportionally distributed throughout the study area (one locality approximately every 30 km). Interview questions concerned fungi species collected, their perceived habitats, and whether any changes had been noted in their abundance. As many as 556 respondents provided information concerning fungal ecology. In these descriptions, 35 taxa were mentioned by at least 5 respondents. Results: The data collected during interviews allowed us to create collective folk descriptions of habitat preferences and a list of 98 different macro-, meso-, and microhabitats of macrofungi described by the respondents. This list of recurring habitats assigned to particular macrofungal taxa coincides with, and sometimes exceeds, data available in scientific publications. Some habitat preferences observed by the informants have not yet been researched or tested by science. Out of 695 respondents, 366 (53%) noticed a steady decrease in local macrofungi abundance, and only one person claimed to have observed a steady increase. Imleria badia was the only species with increased abundance, as noted by fifteen independent respondents. The main listed reason for abundance decrease was drought (f = 186). Conclusions: Collected information on the ecology of fungi shows that local knowledge does not generally diverge from scientific knowledge. The acquired information related to macrofungal abundance and ecology may also be used as a tool for the formulation of new scientific questions and theories. The analysis of local fungi observations might contribute to broadening knowledge about local changes in fungi and enable new estimations related to large-scale analysis of macrofungal abundance.
... In one study, the composition of ectomycorrhizal fungal communities was altered, but only a small proportion of the fungi appeared to be strongly sensitive to warming (Mucha et al. 2018). In another study, it was observed that warming leads to a decline in the photosynthetic rate of boreal forest trees, again associated with a shift towards fewer carbon-demanding symbiotic mycorrhizal fungi (Fernandez et al. 2017). ...
Technical Report
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In this report, we summarize the current state of knowledge and best estimates of how climate change is expected to impact Norwegian forest ecosystems from now to the year 2100
... Community shifts and the selectivity of EcMF response were revealed again. The benefit to short-contact exploration strategists provided by warming under condition of suppressed host photosynthesis were revealed which can be explained with a selection towards less C demanding EcMF (Fernandez et al., 2017). The observed advance of any EcMF exploration strategy is inconsistent across different studies, e.g., medium distance exploration type turned out to prevail in Arctic Alaskan tundra under temperature elevation (Morgado et al., 2015), but the warming-driven shifts in EcMF extraradical part are reported regularly. ...
Chapter
Global change is expected to affect fungi both directly and through associated organisms. Due to ubiquity and many-sided ecosystem roles, fungi can largely contribute to ecosystem resilience under negative impacts, thus their responses to warming, extreme weather events, carbon dioxide and nitrogen-elevated concentrations are essential. Fungal responses to climate change factors are hard to discriminate from non-climatic ones because of retaining gaps in fungal ecology and geography and huge variety across taxa and functional guilds. Here we present a review of recent data on different groups of terrestrial saprotrophic, mycorrhizal and pathogenic fungi perspectives under climate change with discussing possible mechanisms underlying effects observed or predicted.
... Since fungi belonging to Russula, Cenococcum and Tomentella genera may possess decomposition abilities of complex soil organic matter [15,26,31], our observations might be the result of higher organic matter decomposition rates associated with increased soil temperature under elevated snow cover. The increased abundance of Russula, Cenococcum and Tomentella in response to soil warming has been reported in several studies [30,35,41,65,66]. Increased snow cover at the wet tundra site positively affected saprotrophic Mycena and Clavaria. ...
Article
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Background Climate models predict substantial changes in temperature and precipitation patterns across Arctic regions, including increased winter precipitation as snow in the near future. Soil microorganisms are considered key players in organic matter decomposition and regulation of biogeochemical cycles. However, current knowledge regarding their response to future climate changes is limited. Here, we explore the short-term effect of increased snow cover on soil fungal, bacterial and archaeal communities in two tundra sites with contrasting water regimes in Greenland. In order to assess seasonal variation of microbial communities, we collected soil samples four times during the plant-growing season. Results The analysis revealed that soil microbial communities from two tundra sites differed from each other due to contrasting soil chemical properties. Fungal communities showed higher richness at the dry site whereas richness of prokaryotes was higher at the wet tundra site. We demonstrated that fungal and bacterial communities at both sites were significantly affected by short-term increased snow cover manipulation. Our results showed that fungal community composition was more affected by deeper snow cover compared to prokaryotes. The fungal communities showed changes in both taxonomic and ecological groups in response to climate manipulation. However, the changes were not pronounced at all sampling times which points to the need of multiple sampling in ecosystems where environmental factors show seasonal variation. Further, we showed that effects of increased snow cover were manifested after snow had melted. Conclusions We demonstrated rapid response of soil fungal and bacterial communities to short-term climate manipulation simulating increased winter precipitation at two tundra sites. In particular, we provide evidence that fungal community composition was more affected by increased snow cover compared to prokaryotes indicating fast adaptability to changing environmental conditions. Since fungi are considered the main decomposers of complex organic matter in terrestrial ecosystems, the stronger response of fungal communities may have implications for organic matter turnover in tundra soils under future climate.
... The differences in the fungal community among treatments are mainly due to changes in the relative abundance of Ascomycetes (Table 3). The relative abundance of ectomycorhizal fungal Ascomycetes is found to be inversely correlated with the photosynthetic rate of host plants (Fernandez et al., 2017). The increase in AGB but no difference in BGB (Fig. 1) can ensure enough root exudates to supply the C demand of Ascomycetes. ...
Article
The response of soil microbial decomposition of soil organic carbon (C) to temperature variation against an average warming background is of great importance to understand how climate change affects the ecosystem C cycling. In this study, a warming and step-wised stop-warming experiment was conducted to examine whether the response of soil respiration (Rs) and heterotrophic respiration (Rh) persists post-warming and to understand the underlying mechanisms. The treatment plots (10 plots) were warmed (~1.5 °C at 10 cm soil depth) in 2017, then warming was stopped in one group (5 plots) in 2018 (WS18) and stopped in another group (the remaining 5 plots) in 2019 (WS19). Plant biomass, soil microbial biomass, and soil microbial community composition were measured from 2017 to 2019.On average, warming increased Rh by 28% in 2017. The Rh in WS18 was stilled increased by 26% in 2018, which was lower than the warming induced increase in Rh in WS19 at the same period. The Rh in WS18 showed no difference with the control and that in WS19 was higher than the control in only June in 2019. Aboveground biomass of WS18 and WS19 increased by 20% and 29%, respectively in 2017, and they were still increased by 12% and 17% in 2019 even the warming stopped one two years and one years, respectively. Belowground biomass, microbial biomass, and diversity indices showed no significant differences among treatments in 2018 or 2019. The fungal community was significantly different among WS18, W19, and the control in both 2018 and 2019. The relative abundance of Ascomycetes, which made the largest contribution to the differences in the fungal community, was negatively correlated with Rh (r = −0.4, n = 30, p < 0.05). Our results indicate a warming legacy effect on the microbial decomposition of soil organic C, resulting from the increase in plant productivity and fungal community change when warming stopped.
... Moreover, ECM fungi can facilitate the establishment of late-succession trees (Booth, 2004;Nara and Hogetsu, 2004). Ectomycorrhizal fungi are thus major actors in forest dynamics and may also affect host tolerance to climate change (Fernandez et al., 2016;Mucha et al., 2018). ...
Thesis
Au Québec, le 49° de latitude nord représente la frontière entre d'une part la forêt mixte dominée par le sapin baumier et le bouleau et d'autre par la forêt boréale dominée par l'épinette noire. Cette frontière tend à migrer vers le nord avec la migration du sapin. Dans les plaines argileuses de l'Abitibi-Témiscamingue qui se trouvent à cette latitude, le sapin possède localement une meilleure capacité d'établissement sous les couverts dominés par le peuplier faux-tremble en comparaison à ceux dominés par l'épinette noire. Les conditions climatiques et édaphiques sont similaires dans les deux types de peuplement, mais les conditions biotiques diffèrent. Le sous-bois sous épinette est dominé par les mousses et des arbustes de la famille des éricacées, tandis que le sous-bois associé aux peuplements de peupliers présente une richesse spécifique plus élevée, plus particulièrement en espèces arbustives et herbacées. Les communautés végétales des strates arborées et de sous-bois sont connues pour affecter les communautés fongiques du sol et notamment les communautés mycorhiziennes. Or, ces dernières pourraient expliquer les différences d'établissement du sapin observées entre les deux types de peuplement. En effet, les mycorhizes sont des symbioses à bénéfices réciproques entre des champignons et les racines des arbres et elles sont particulièrement importantes pour la nutrition des plantes en forêt boréale. Cependant, il y a très peu d'informations sur les mycorhizes dans le système boréal québécois relativement à la Scandinavie ou l'Alaska. Dans ce projet, nous avons testé 1) si les communautés de champignons du sol sont différentes entre les peuplements de peuplier et d'épinette, 2) si les sapins s'associent avec un plus grand nombre d'espèces de champignons, mais aussi à des espèces différentes sous les peupliers et 3) si les symbioses mises en place sous les peupliers sont plus efficaces que celles sous les épinettes pour la nutrition du sapin. Le séquençage haut débit de l'ADN des champignons du sol a permis de détecter une forte diversité fongique et de mettre en évidence des différences dans la composition des communautés fongiques du peuplier et de l'épinette, aussi bien pour les champignons décomposeurs que pour les champignons mycorhiziens. Pendant deux années, soixante jeunes plants de sapins ont été suivis sur le terrain afin de relier la croissance et le taux de nutriments dans les aiguilles (deux estimateurs de la vigueur) au taux de mycorhization et à la diversité fongique. L'analyse a révélé que le taux de nutriments dans les aiguilles du sapin était supérieur sous les peupliers par rapport au sapin poussant sous les épinettes à proximité de plantes éricacées. De plus, la présence des plantes éricacées était corrélée à des changements de la communauté fongique mycorhizienne associée aux racines du sapin, ainsi qu'à une diminution du contenu en azote dans les aiguilles. Des expériences ont également été menées en chambre de croissance afin de déterminer si la mycorhization avait un impact sur la germination, la survie, la nutrition et la croissance des jeunes plantules. Pour ce faire, des sapins ont été semés dans des sols organiques et minéraux provenant des différents types de peuplement et la moitié a été stérilisée afin d'éliminer les microorganismes. Les résultats obtenus après trois saisons de croissance ont permis de détecter un effet de l'identité des microorganismes du sol plutôt qu'un effet du taux de mycorhization sur la nutrition et la croissance du sapin. De plus, les sapins poussant dans les sols récoltés sous épinette mais à distance des éricacées ont eu une meilleure nutrition azotée que dans les sols prélevés sous peuplier.
... Climate treatments sharing the same letters are not significantly different. (Fernandez et al., 2017) under more arid conditions. Climatically stressed survivor EM plants may instead be forced to rely on direct root nutrient uptake or other less carbon-demanding symbiotic partners such as ascomycete EMF with contact or short-distance hyphal exploration types and less complex enzymatic capabilities (Geopora). ...
Article
Full-text available
The aboveground impacts of climate change receive extensive research attention, but climate change could also alter belowground processes such as the delicate balance between free-living fungal decomposers and nutrient scavenging ectomycorrhizal fungi (EMF) that can inhibit decomposition through a mechanism called the Gadgil effect. We investigated how climate change-induced reductions in plant productivity alter soil fungal community composition in a semiarid shrubland exposed to experimental warming (W) and/or rainfall reduction (RR). We hypothesized that reductions in photosynthesis and plant nutrient demand under a warmer and drier climate will decrease EMF abundance, thereby favouring the proliferation and activity of fungal saprotrophs. The relative abundance of EMF sequences decreased by 57.5% under W+RR, which was accompanied by reductions in the activity of extracellular hydrolytic enzymes involved in the acquisition of organic-bound nitrogen and phosphorus by EMF and their host plants. This created an enhanced potential for soil organic matter (SOM) breakdown and nitrogen-mineralization by fungal decomposers, as revealed by 2/3-fold increases in dissolved organic carbon and nitrogen and decreasing SOM content through time. Climate change impacts on vegetation can cascade belowground through shifts in soil fungal guild structure that alter ecosystem biogeochemical functioning and accelerate SOM decomposition by reducing the Gadgil effect.
... For example, drought and elevated CO 2 generally enhance the allocation of root biomass over shoot biomass for acquiring both water and nutrients 3 , whereas increased precipitation and nitrogen deposition usually elevate shoot biomass allocation for increased competition for light 4,5 . Climate warming has also been shown to affect net primary production in terrestrial ecosystem, such as by increasing biomass production [6][7][8] , which is further shown to trigger higher demands for resources by plants 9,10 . Accordingly, warming effects on R/S may depend on temperature effects on resource supply, which makes it challenging to predict warming effects on plant's biomass allocations, particularly at a global scale 11,12 . ...
Preprint
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Biomass allocation in plants is fundamental for understanding and predicting terrestrial carbon storage. Recent studies suggest that climate warming can differentially affect root and shoot biomass, and subsequently alter root: shoot ratio. However, warming effects on root: shoot ratio and their underlying drivers at a global scale remain unclear. Using a global synthesis of >300 studies, we here show that warming significantly increases biomass allocation to roots (by 13.1%), and two factors drive this response: mean annual precipitation of the site, and the type of mycorrhizal fungi associated with a plant. Warming-induced allocation to roots is greater in relatively drier habitats compared to shoots (by 15.1%), but lower in wetter sites (by 4.9%), especially for plants associated with arbuscular mycorrhizal fungi compared to ectomycorrhizal fungi. Root-biomass responses to warming predominantly determine the biomass allocation in terrestrial plants suggesting that warming can reinforce the importance of belowground resource uptake. Our study highlights that the wetness or dryness of a site and plants’ mycorrhizal associations strongly regulate terrestrial carbon cycle by altering biomass allocation strategies in a warmer world.
... arbuscular and ericoid mycorrhizal fungi), and pathotrophic guild modes using FUNGUILD (Nguyen et al., 2016). When possible, the top 50 most abundant unassigned OTUs (due to missing genus taxonomy) were assigned manually to either EM or saprotrophic guilds using criteria detailed in Fernandez et al. (2017). A list of guild assignments is provided in Table S3. ...
Article
Interactions between symbiotic ectomycorrhizal (EM) and free‐living saprotrophs can result in significant deceleration of leaf litter decomposition. While this phenomenon is widely cited, its generality remains unclear, as both the direction and magnitude of EM fungal effects on leaf litter decomposition have been shown to vary among studies. Here we explicitly examine how contrasting leaf litter types and EM fungal communities may lead to differential effects on carbon (C) and nitrogen (N) cycling. Specifically, we measured the response of soil nutrient cycling, litter decay rates, litter chemistry and fungal community structure to the reduction of EM fungi (via trenching) with a reciprocal litter transplant experiment in adjacent Pinus‐ or Quercus‐dominated sites. We found clear evidence of EM fungal suppression of C and N cycling in the Pinus‐dominated site, but no suppression in the Quercus‐dominated site. Additionally, in the Pinus‐dominated site, only the Pinus litter decay rates were decelerated by EM fungi and were associated with decoupling of litter C and N cycling. Our results support the hypothesis that EM fungi can decelerate C cycling via N competition, but strongly suggest that the ‘Gadgil effect’ is dependent on both substrate quality and EM fungal community composition. We argue that understanding tree host traits as well as EM fungal functional diversity is critical to a more mechanistic understanding of how EM fungi mediate forest soil biogeochemical cycling.
... Similarly, mycorrhizal fungal diversity is often impacted rather quickly by global change, but the effects are not consistent. For example, warming can increase (Deslippe et al., 2012), have no effect on (Fernandez et al., 2017), or decrease (Geml et al., 2015) EM fungal richness. Similarly, AM fungal richness sometimes increases (Yang et al., 2013;Kim et al., 2015), but also decreases (Cao et al., 2020) under long-term warming. ...
Article
Full-text available
First principles predict that diversity at one trophic level often begets diversity at other levels, suggesting plant and mycorrhizal fungal diversity should be coupled. Local-scale studies have shown positive coupling between the two, but the association is less consistent when extended to larger spatial and temporal scales. These inconsistencies are likely due to divergent relationships of different mycorrhizal fungal guilds to plant diversity, scale dependency, and a lack of coordinated sampling efforts. Given that mycorrhizal fungi play a central role in plant productivity and nutrient cycling, as well as ecosystem responses to global change, an improved understanding of the coupling between plant and mycorrhizal fungal diversity across-scales will reduce uncertainties in predicting the ecosystem consequences of species gains and losses.
... Climate treatments sharing the same letters are not significantly different. (2021) (Fernandez et al., 2017) under more arid conditions. Climatically stressed survivor EM plants may instead be forced to rely on direct root nutrient uptake or other less carbon-demanding symbiotic partners such as ascomycete EMF with contact or short-distance hyphal exploration types and less complex enzymatic capabilities (Geopora). ...
Article
Full-text available
The aboveground impacts of climate change receive extensive research attention, but climate change could also alter belowground processes such as the delicate balance between free-living fungal decomposers and nutrient-scavenging mycorrhizal fungi that can inhibit decomposition through a mechanism called the Gadgil effect. We investigated how climate change-induced reductions in plant survival, photosynthesis and productivity alter soil fungal community composition in a mixed arbuscular/ectomycorrhizal (AM/EM) semiarid shrubland exposed to experimental warming (W) and/or rainfall reduction (RR). We hypothesised that increased EM host plant mortality under a warmer and drier climate might decrease ectomycorrhizal fungal (EMF) abundance, thereby favouring the proliferation and activity of fungal saprotrophs. The relative abundance of EMF sequences decreased by 57.5% under W+RR, which was accompanied by reductions in the activity of hydrolytic enzymes involved in the acquisition of organic-bound nutrients by EMF and their host plants. W+RR thereby created an enhanced potential for soil organic matter (SOM) breakdown and nitrogen mineralisation by decomposers, as revealed by 127–190% increases in dissolved organic carbon and nitrogen, respectively, and decreasing SOM content in soil. Climate aridification impacts on vegetation can cascade belowground through shifts in fungal guild structure that alter ecosystem biogeochemistry and accelerate SOM decomposition by reducing the Gadgil effect.
... climate, plant category) across studies. This analysis was conducted in two ways: (i) by testing for relationships using the relative abundance of fungi identified to the phylum level and the genus level without accounting for phylogenetic relatedness (Fernandez et al. 2017) and then (ii) testing for a phylogenetic signal to preferred decay stage of each fungal genus (Mönkkönen et al. 2011;Treseder et al. 2014;Norros and Halme 2017). For the first (non-phylogenetic) analysis, we regressed relative abundance of fungal taxa against % mass loss using a random effects generalized linear multiple regression model (Yee and Mitchell 1991) that is commonly used to model relative abundance data (Warton et al. 2015). ...
Article
Full-text available
Ecologists have frequently observed a pattern of fungal succession during litter decomposition, wherein different fungal taxa dominate different stages of decay in individual ecosystems. However, it is unclear which biological features of fungi give rise to this pattern. We tested a longstanding hypothesis that fungal succession depends on the evolutionary history of species, such that different fungal phyla prefer different decay stages. To test this hypothesis, we performed a meta-analysis across studies in 22 different ecosystem types to synthesize fungal decomposer abundances at early, middle and late stages of plant litter decay. Fungal phyla varied in relative abundance throughout decay, with fungi in the Ascomycota reaching highest relative abundance during early stages of decay (P < 0.001) and fungi in the Zygomycota reaching highest relative abundance during late stages of decay (P < 0.001). The best multiple regression model to explain variation in abundance of these fungal phyla during decay included decay stage, as well as plant litter type and climate factors. Most variation in decay-stage preference of fungal taxa was observed at basal taxonomic levels (phylum and class) rather than finer taxonomic levels (e.g. genus). For many finer-scale taxonomic groups and functional groups of fungi, plant litter type and climate factors were better correlates with relative abundance than decay stage per se, suggesting that the patchiness of fungal community composition in space is related to both resource and climate niches of different fungal taxa. Our study indicates that decomposer fungal succession is partially rooted in fungal decomposers' deep evolutionary history, traceable to the divergence among phyla.
... The impacts of global climate change and other anthropogenic activities on the structure and function of fungal communities in Canada is not currently known, making it difficult to predict their effects on future landscapes. Fungi are especially sensitive to climate change (Körner 2003;Giauque and Hawkes 2013;Kivlin et al. 2013;Fernandez et al. 2017;Andrew et al. 2018aAndrew et al. , 2018b and atmospheric pollution, including nitrogen deposition (Treseder 2004;Lilleskov et al. 2011;Allen and Allen 2017;van Strien et al. 2018); changing or extreme weather patterns due to global warming may lead to fruiting body declines and shifts in phenology (Gange et al. 2007;Kauserud et al. 2012;Boddy et al. 2014;Gange et al. 2018). ...
Article
Full-text available
Despite the ecological importance of fungi, we still know little about their diversity in Canada. One of the largest hurdles to implementing fungal conservation initiatives is the lack of fungal distribution data. As anthropogenic impacts accelerate the speed of environmental change, it is imperative that we fill this major information gap, critical for fungal protection. To gain insight on the conservation status of Canadian macrofungi, we took advantage of the large and growing body of fungal biodiversity data from government research ( Wild Species 2020), citizen science, trained independent mycologists, university, and museum biodiversity research. The majority of macrofungi are data deficient; we do not know their geographic distribution or habitat requirements, occurrence, or abundance in Canada. For mushrooms that fruit only a few days of the year and are often difficult to positively identify, there is a lot of work to overcome the uncertainty of distinguishing under-sampling from rarity. Our work stresses the importance of building a strong network of professional and amateur mycologists to develop resources, disseminate information to make educated decisions, and advance conservation actions. We found that several fungi can be prioritized; we present a short list for consideration for formal conservation assessment.
... Although many functions can be performed by Python and Bash scripting, the process of checking taxonomic annotations based on multiple best hits needs to be performed manually because the first hit may be incompletely annotated and curated reference databases still contain some misassigned data. Often, representative sequences require BLAST-based reanalysis against INSDc for taxonomic determination, more complete functional annotation (Fernandez et al., 2017) or additional chimera control using the graphic summary view (Nilsson et al., 2012). ...
Article
Full-text available
The development of high‐throughput sequencing (HTS) technologies has greatly improved our capacity to identify fungi and unveil their ecological roles across a variety of ecosystems. Here we provide an overview of current best practices in metabarcoding analysis of fungal communities, from experimental design through molecular and computational analyses. By re‐analysing published datasets, we demonstrate that operational taxonomic units (OTUs) outperform amplified sequence variants (ASVs) in recovering fungal diversity, a finding that is particularly evident for long markers. Additionally, analysis of the full‐length ITS region allows more accurate taxonomic placement of fungi and other eukaryotes compared to the ITS2 subregion. Finally, we show that specific methods for compositional data analyses provide more reliable estimates of shifts in community structure. We conclude that metabarcoding analyses of fungi are especially promising for integrating fungi into the full microbiome and broader ecosystem functioning context, recovery of novel fungal lineages and ancient organisms as well as barcoding of old specimens including type material.
... Some root-associated fungi have negative effects on plants, such as pathogenic fungi, which can cause severe plant diseases resulting in decreased plant biomass, whereas plant mutualists, such as mycorrhizal fungi, can enhance plant nutrient uptake and improve disease resistance (van der Heijden et al. 2006). Many studies have focused on the impact of climate warming on specific fungal groups, such as arbuscular mycorrhizal fungi (Birgander et al. 2017) or ectomycorrhizal fungi (Fernandez et al. 2017), yet disparate fungal groups could colonize the same segment of plant roots. There is evidence that different groups of root-associated fungi respond differently to climate change (Olsrud et al. 2009), and distinct environmental conditions could switch the interaction between different fungal groups from cooperative to antagonistic (Abrego et al. 2020a, b;Faust and Raes 2012). ...
Article
Full-text available
Background and aimsRoot-associated fungi link resource fluxes between the soil and roots, thus influencing plant growth and ecosystem function. However, at present, the impact of global warming on these fungi and their plant host specialization, especially in ecosystems on the Qinghai-Tibetan Plateau is obscure.Methods Here, pot experiments were conducted to examine the root-associated fungal community structure of 14 host plant species undergoing two years of experimental warming on the Qinghai-Tibetan Plateau. Infrared heaters were used to raise the soil temperature to 2.0 ℃ higher than the relative ambient temperature. Subsequently, the endophytic and rhizoplane fungal communities were explored by sequencing the fungal internal transcribed spacer (ITS) region.ResultsA total of 1564 OTUs were identified, which were dominated by ascomycetes (82.71%). Similar root-associated fungal diversity and community composition were identified under ambient and warming environments. The root-associated fungal community composition significantly varied among different host plant species, and this dissimilarity was enhanced under experimental warming. Root N concentration was essential in shaping the structure of the root-associated fungal community.Conclusions Although the root-associated fungal community was resilient to short-term warming, our study highlights that climate warming can induce higher host specificity of root-associated fungal communities in the alpine meadow ecosystem.
Article
Ectomycorrhizal (ECM) fungal communities show temporal dynamics. Such dynamics have been mainly assessed with one year of investigations and have been related to the seasonal changes in environment. Recent study in sub-tropical region has revealed that stochastic temporal-based process can affect ECM fungal community, making the community of the same season different between years. The different community structures across years have also been observed in the Arctic region with a grass host. Nevertheless, in temperate zones, the effect of temporal-based processes and the consistency of seasonal dynamics have never been investigated. We conducted a two-year root sampling in a cool temperate Fagus crenata forest to test whether the temporal variation of ECM fungal community composition could be explained by season. The explanation powers of temporal distance and environmental factors for the temporal dynamics of ECM fungal community were simultaneously evaluated. The variation in community structure was significantly explained by year but not by season, indicating that seasonal community structure differed between years. This difference in the community structure across years was partly explained by temporal factors. Our study implies that the temporal dynamics of ECM fungal communities in temperate forests are affected by temporal-based factors and can vary across years.
Article
With the continual improvement of high‐throughput sequencing technology and constant updates to fungal reference databases, the use of amplicon‐based DNA markers as a tool to reveal fungal diversity and composition in various ecosystems has become feasible. However, both primer selection and experimental procedure still require meticulous verification. Here, we computationally and experimentally evaluated the accuracy and specificity of three widely used or newly designed internal transcribed spacer (ITS) primer sets (ITS1F/ITS2, gITS7/ITS4 and 5.8S‐Fun/ITS4‐Fun). In silico evaluation revealed that the primer coverage varied at different taxonomy levels due to the differences in degeneracy and location of primer sets. Using even and staggered mock community standards, we identified different proportions of chimeric and mismatch reads generated by different primer sets, as well as great variation in species abundances, suggesting that primer selection would affect the results of amplicon‐based metabarcoding studies. Choosing a proofreading and high‐fidelity polymerase (KAPA HiFi) could significantly reduce the percentage of chimeric and mismatch sequences, further reducing OTU inflation. Moreover, for two types of environmental fungal communities, plant endophytic and soil fungi, it was demonstrated that the three primer sets could not reach a consensus on fungal community compositions or diversities, and primer selection, not the experimental treatment, determines observed soil fungal community diversity and composition. Future DNA marker surveys should pay greater attention to potential primer effects and improve the experimental scheme to increase credibility and accuracy.
Article
The response to global change by soil microbes is set to affect important ecosystem processes. These impacts could be most immediate in transitional zones, such as the temperate-boreal forest ecotone, yet previous work in these forests has primarily focused on specific subsets of microbial taxa. Here, we examined how bacterial and fungal communities respond to simulated above- and belowground warming under realistic field conditions in closed and open canopy treatments in Minnesota, USA. Our results show that warming and canopy disturbance shifted bacterial and fungal community structure as dominant bacterial and fungal groups differed in the direction and intensity of their responses. Ectomycorrhizal and saprotrophic fungal communities with greater connectivity (higher prevalence of strongly interconnected taxa based on pairwise co-occurrence relationships) were more resistant to compositional change. Warming effects on soil enzymes involved in the hydrolytic and oxidative liberation of carbon from plant cell walls and nutrients from organic matter were most strongly linked to fungal community responses, although community structure-function relationships differed between fungal guilds. Collectively, these findings indicate that warming and disturbance will influence the composition and function of microbial communities in the temperate-boreal ecotone, and fungal responses are particularly important to understand for predicting future ecosystem functioning.
Article
Disordered germination is widely observed in plant species with extremely small populations (PSESPs) in China. Abies beshanzuensis M. H. Wu, a PSESP (with only three extant adults in Zhejiang Province, China) that also has poor seed germination in the field, belongs to the Pinaceae family. Pinaceae generally tend toward symbiosis with ectomycorrhizal (ECM) fungi to alleviate climate change-induced stresses. Therefore, exploring how to improve seed germination of A. beshanzuensis and whether it is an ECM species will contribute to increasing recruitment for conducting further conservation research. In this study, four temperature regimes (10/15 °C, 15/20 °C, 20/25 °C, and 25/30 °C) were selected to explore the response of seed germination to rising temperature. Based on the microscopic features of fine roots, together with molecular techniques, the mycorrhizal type of this species was identified. The seed germination of A. beshanzuensis was increased from 1–2% to around 4.5% by 14-day cold stratification and under 20/25 °C fluctuating temperature conditions. Our findings indicated that A. beshanzuensis may be endangered as a result of insufficient seedling recruitment due to poor germination under the current climate. A. beshanzuensis was confirmed as an ECM fungi-associated tree species. This study highlights the necessity of incorporating auxiliary seed treatment into population recovery programs of A. beshanzuensis, thereby better conserving the species under ongoing environmental changes.
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Fungi are key players in vital ecosystem services, spanning carbon cycling, decomposition, symbiotic associations with cultivated and wild plants and pathogenicity. the high importance of fungi in ecosystem processes contrasts with the incompleteness of our understanding of the patterns of fungal biogeography and the environmental factors that drive those patterns. to reduce this gap of knowledge, we collected and validated data published on the composition of soil fungal communities in terrestrial environments including soil and plant-associated habitats and made them publicly accessible through a user interface at https://globalfungi.com. The GlobalFungi database contains over 600 million observations of fungal sequences across > 17 000 samples with geographical locations and additional metadata contained in 178 original studies with millions of unique nucleotide sequences (sequence variants) of the fungal internal transcribed spacers (ITS) 1 and 2 representing fungal species and genera. the study represents the most comprehensive atlas of global fungal distribution, and it is framed in such a way that third-party data addition is possible.
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Forest disturbances have a strong effect on soil fungal communities and associated ecosystem processes. However, little is known about the response of mycelial biomass to disturbances, and how fungi reallocate carbon into different fungal structures under environmental stressors. We investigated above- and below-ground fungal biomass shifts in response to different intensities of forest management in Mediterranean Pinus pinaster forests. Soil fungal biomass was estimated by ergosterol quantification and production of sporocarps was estimated from repeated field samplings during 5 years in 26 experimental plots. Abundance of mycorrhizal and saprotrophic fungi belowground was determined using Pacific Biosciences sequencing of fungal ITS2 amplicons. Thinning had a prolonged negative effect belowground, inter- and intra-annually, on total fungal biomass and on the biomass of ectomycorrhizal fungi, but not on saprotrophic fungi. Total and ectomycorrhizal mushroom yields were negatively correlated with the total and the ectomycorrhizal mycelial biomass, respectively. Thinning also correlated positively with the aboveground/belowground ratio of both total and ectomycorrhizal fungal biomass. We show potential short-term shifts in resource allocation of fungi from below-to above-ground structures under disturbances such as forest thinning. Ectomycorrhizal fungi may respond to disturbances by increasing reproduction rather than colonizing the surrounding soil.
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The cultivation of plantation forests is likely to change the diversity and composition of soil fungal communities. At present, there is scant information about these communities in Ethiopian plantation forest systems. We assessed the soil fungal communities in Pinus patula Schiede ex Schltdl. & Cham. stands aged 5, 11, or 36-years-old using DNA metabarcoding of ITS2 amplicons. The ecological conditions of each plot, such as climate, altitude, and soil, were similar. Stand age and soil fertility influenced soil fungal species diversity and ecological guilds. In total, 2262 fungal operational taxonomic units were identified, of which 2% were ectomycorrhizal (ECM). The diversity of ECM fungi was higher in the 5 and 36-year-old stands than in the 11-year-old P. patula stands. Contrary to our expectations, a high level of ECM species diversity was observed in young stands, suggesting that these ECM species could compensate for the effects of nutrient stress in these stands. Our results also suggested that the abundance of plant pathogens and saprotrophs was not affected by stand age. This study provides baseline information about fungal community changes across tree stands of different ages in P. patula plantations in Ethiopia that are likely related to ECM fungi in young stands where relatively low soil fertility prevails. However, given that the plots were established in a single stand for each age class for each treatment, this study should be considered as a case study and, therefore, caution should be exercised when applying the conclusions to other stands.
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Plant nutrient acquisition strategies involving ectomycorrhizal (EcM) and arbuscular mycorrhizal (AM) associations, are key plant functional traits leading to distinct carbon (C) and nutrient dynamics in forests. Yet, little is known about how these strategies influence the structure and functioning of soil communities, and if such mycorrhizal effects may be more or less pronounced depending on the type of forest and various abiotic factors. Here we explore the potential interactions occurring between plant-EcM and plant-AM systems with the diverse soil organisms occurring in forest soils, and in the process draw attention to major issues that are worthy for future research directions. Based on these potential interactions, we suggest that EcM systems, especially those involving gymnosperms in colder climates, may select for a soil community with a narrow set of functions. These EcM systems may exhibit low functional redundancy, dominated by symbiotic interactions, where EcM fungi maintain low pH and high C/N conditions in order to tightly control nutrient cycling and maintain the dominance of EcM trees. By contrast, AM systems, particularly those involving deciduous angiosperm trees in mild and warmer climates, may facilitate a functionally more diverse and redundant soil community tending towards the dominance of competitive and antagonistic interactions, but also with a range of symbiotic interactions that together maintain diverse plant communities. We propose that the contrasting belowground interactions in AM and EcM systems act as extended nutrient acquisition traits that contribute greatly to the prevailing nutrient and C dynamics occurring in these systems.
Article
Forests have expanded across Europe over the last centuries as a consequence of farmland (agricultural and pasture) abandonment. Agricultural practices usually increase soil fertility and reduce the diversity and abundance of ectomycorrhizal (ECM) fungi, essential mutualists of many woody species in temperate and Mediterranean forests. The recovery of this biotic interaction after the cessation of human activities is, thus, crucial for the re‐establishment of functional forest ecosystems. Here we addressed the legacies of past land use and the recovery of the mutualism between ECM fungi and Fagus sylvatica trees in recent beech forests (< 50 years) in Northeast Spain. Soil and root samples were collected in 6 long‐established and 8 recent beech forests to analyse soil abiotic properties and the ECM fungi associated with beech roots (Illumina DNA metabarcoding of ECM tips). Up to 609 amplicon sequence variants (ASV) of ECM fungi were identified, with 220 ASV found in both forest types. Recent forests had a significantly lower soil organic matter and phosphorus content, which had a significant effect on the community structure of ECM fungi in beech roots. Moreover, beech trees in recent forests interacted with less fungal taxa but had a higher relative abundance of Ascomycota. Tarzetta spp. (Ascomycota, Pezizales) and Lactarius blennius (Basidiomycota, Russulales) emerges as the particular taxa associated with recent and long‐established forests, respectively. More specialized mutualistic networks with a lower species normalized degree were found in recent forests, which might result in a lower quality and resilience of the ectomycorrhizal mutualism. Synthesis: Land‐use history modulated the mycorrhizal symbioses in regenerating beech forests through changes in soil organic matter and nitrogen, which were the main drivers of the differences in fungal community composition and functional types associated with beech trees in recent forests.
Thesis
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The main objective of this thesis was to understand, describe and quantify the coupled effects of forest thinning, tree growth and climate on fungal biomass, productivity and community composition. To this end, huge amount of dataset from different disciplines has been compiled during several years (mid- to long-term) and at different spatial scales across Europe, covering in turn manifold approaches: mycological data, dendrochronological information, climatic data and forest stand parameters. The results showed that: (i) only under more water-limited conditions, both the tree growth and the mushroom productivity are more sensitive to precipitation events, resulting in higher synchrony between both processes; (ii) models may be used to reconstruct mushroom production along historical periods based on dendrochronological information, but also to predict future mushroom yields based on climate-sensitive tree and stand growth predictions; (iii) forest thinning may cause potential short-term shifts in resource allocation of fungi from below- to above-ground structures; and (iv) forest thinning practices with a careful removal of trees does not compromise the sporocarp diversity, but lead to short-term successional changes in fungal assemblages. http://hdl.handle.net/10803/671578
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Mediterranean forest dynamics are tightly linked to belowground fungal communities since fungi are involved in key ecosystem processes such as organic matter and nutrient cycling, water regulation, soil preservation or mutualistic associations. The latter is particularly important for tree species such as pines that need to establish symbioses with mycorrhizal fungi for survival and development. Mycorrhizal fungi improve water and nutrient uptake by the host tree, in exchange for photosynthetic carbohydrates, directly affecting the productivity and the response of trees to the surrounding environment. This close mutualistic association with fungi helps trees cope with the limiting environmental conditions often found in Mediterranean areas, which can be particularly relevant in the context of global change. Forests provide multiple provisioning (timber, mushrooms, food, fuel), cultural (recreation space, landscape), regulatory (carbon sequestration, air and water purification) and supporting (soil formation, primary production, nutrient cycling) ecosystem services. Moreover, soil fungal diversity promotes multiple ecosystem functions, e.g., decomposition, mineralization, and nutrient cycling, ensuring the delivery of key regulatory ecosystem services in forests. Mushroom harvesting is highly valued in the Mediterranean region and the integration of mushroom and truffle production in forest management strategies is of paramount importance.
Article
Increasing temperature and decreasing precipitation has led to more frequent and extreme drought events in many regions throughout the world. In the western United States, multi‐year drought events have led to widespread plant mortality and extreme wildfires (Asner et al. 2016, Pickrell and Pennisi 2020). Communities of ectomycorrhizal fungi (EMF) ‐ root symbionts which play a critical role in forest health ‐ are also thought to be threatened by these climatic changes (Fernandez et al. 2017, Steidinger et al. 2019). However, altered soil moisture conditions have complex direct and indirect effects on both fungi and ecosystem processes, such as nutrient availability (Schimel 2018), making it difficult to elucidate the primary drivers of community composition based on field observations or experiments (Pena and Polle 2014). As a result, efforts to identify the genes or traits involved in response to drought events are critical for accurate prediction of future EMF composition and function (Allison and Treseder 2008, Romero‐Olivares et al. 2019). Despite this fact, we are not aware of any studies that have used gene expression analyses to measure the response of individual EMF to drought events or other climatic stressors.
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The rise in wildfire frequency in the western United States has increased interest in secondary succession. However, despite the role of soil microbial communities in plant regeneration and establishment, microbial secondary succession is poorly understood owing to a lack of measurements immediately post-fire and at high temporal resolution. To fill this knowledge gap, we collected soils at 2 and 3 weeks and 1, 2, 3, 4, 6, 9, and 12 months after a chaparral wildfire in Southern California. We assessed bacterial and fungal biomass with qPCR of 16S and 18S and richness and composition with Illumina MiSeq sequencing of the 16S and ITS2 amplicons. We found that fire severely reduced bacterial biomass by 47% and richness by 46%, but the impacts were stronger for fungi, with biomass decreasing by 86% and richness by 68%. These declines persisted for the entire post-fire year, but bacterial biomass and richness oscillated in response to precipitation, whereas fungal biomass and richness did not. Fungi and bacteria experienced rapid succession, with 5-6 compositional turnover periods. As with plants, fast-growing surviving microbes drove successional dynamics. For bacteria, succession was driven by the phyla Firmicutes and Proteobacteria, with the Proteobacteria Massilia dominating all successional time points, and the Firmicutes (Domibacillus and Paenibacillus) dominating early- to mid-successional stages (1-4.5 months), while the Proteobacteria Noviherbaspirillum dominated late successional stages (4.5-1 year). For fungi, succession was driven by the phyla Ascomycota, but ectomycorrhizal basidiomycetes, and the heat-resistant yeast, Geminibasidium were present in the early successional stages (1 month). However, pyrophilous filamentous Ascomycetes Pyronema, Penicillium, and Aspergillus, dominated all post-fire time points. While wildfires vastly decrease bacterial and fungal biomass and richness, similar to plants, pyrophilous bacteria and fungi increase in abundance and experience rapid succession and compositional turnover in the first post-fire year, with potential implications for post-fire chaparral regeneration
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Many trees depend on symbiotic ectomycorrhizal fungi for nutrients in exchange for photosynthetically derived carbohydrates. Trees growing in peatlands, which cover 3% of the earth’s terrestrial surface area yet hold approximately one-third of organic soil carbon stocks, may benefit from ectomycorrhizal fungi that can efficiently forage for nutrients and degrade organic matter using oxidative enzymes such as class II peroxidases. However, such traits may place a higher carbon cost on both the fungi and host tree. To investigate these trade-offs that might structure peatland ectomycorrhizal fungal communities, we sampled black spruce (Picea mariana (Mill.)) seedlings along 100-year-old peatland drainage gradients in Minnesota, USA, that had resulted in higher soil nitrogen and canopy density. Structural equation models revealed that the relative abundance of the dominant ectomycorrhizal fungal genus, Cortinarius, which is known for relatively high fungal biomass coupled with elevated class II peroxidase potential, was negatively linked to site fertility but more positively affected by recent host stem radial growth, suggesting carbon limitation. In contrast, Cenococcum, known for comparatively lower fungal biomass and less class II peroxidase potential, was negatively linked to host stem radial growth and unrelated to site fertility. Like Cortinarius, the estimated relative abundance of class II peroxidase genes in the ectomycorrhizal community was more related to host stem radial growth than site fertility. Our findings indicate a trade-off between symbiont foraging traits and associated carbon costs that consequently structure seedling ectomycorrhizal fungal communities in peatlands.
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Most of the Dry Afromontane forests in the northern part of Ethiopia are located around church territories and, hence, are called church forests. These forests are biodiversity islands and provide key ecosystem services to local communities. A previous study of church forest fungal species was based on sporocarp collections. However, to obtain a complete picture of the fungal community, the total fungal community present in the soil needs to be analyzed. This information is important to integrate church forests into global biodiversity conservation strategies and to understand what actions are required to conserve church forests and their biological components, including fungi, which are known for their exceptionally high diversity levels. We assessed soil fungal communities in three church forests using ITS2 rDNA metabarcoding. In total, 5152 fungal operational taxonomic units representing 16 fungal phyla were identified. Saprotrophs followed by ectomycorrhizal fungi and animal pathogens dominated fungal communities. Significant differences in diversity and richness were observed between forests. Non-metric multidimensional scaling confirmed that fungal community composition differed in each forest. The composition was influenced by climatic, edaphic, vegetation, and spatial variables. Linear relationships were found between tree basal area and the abundance of total fungi and trophic groups. Forest management strategies that consider cover, tree density, enrichment plantations of indigenous host tree species, and environmental factors would offer suitable habitats for fungal diversity, production, and function in these forest systems. The application of the baseline information obtained in this study could assist other countries with similar forest conservation issues due to deforestation and forest fragmentation.
Article
The continuously increasing atmospheric carbon dioxide concentration ([CO2]) has substantial effects on plant growth, and on the composition and structure of forests. However, how plants respond to elevated [CO2] (e[CO2]) under intra- and interspecific competition has been largely overlooked. In this study, we employed Abies faxoniana and Picea purpurea seedlings to explore the effects of e[CO2] (700 ppm) and plant-plant competition on plant growth, physiological and morphological traits, and leaf ultrastructure. We found that e[CO2] stimulated plant growth, photosynthesis and nonstructural carbohydrates (NSC), affected morphological traits and leaf ultrastructure, and enhanced water and nitrogen use efficiencies in A. faxoniana and P. purpurea. Under interspecific competition and e[CO2], P. purpurea showed a higher biomass accumulation, photosynthetic capacity and rate of ectomycorrhizal infection, and higher water and nitrogen use efficiencies compared with A. faxoniana. However, under intraspecific competition and e[CO2], the two conifers showed no differences in biomass accumulation, photosynthetic capacity, and water and nitrogen use efficiencies. In addition, under interspecific competition and e[CO2], A. faxoniana exhibited higher NSC levels in leaves as well as more frequent and greater starch granules, which may indicate carbohydrate limitation. Consequently, we concluded that under interspecific competition, P. purpurea possesses a positive growth and adjustment strategy (e.g., a higher photosynthetic capacity and rate of ectomycorrhizal infection, and higher water and nitrogen use efficiencies), while A. faxoniana likely suffers from carbohydrate limitation to cope with rising [CO2]. Our study highlights that plant-plant competition should be taken into consideration when assessing the impact of rising [CO2] on the plant growth and physiological performance.
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Fungi typically live in highly diverse communities composed of multiple ecological guilds. Although high-throughput sequencing has greatly increased the ability to quantify the diversity of fungi in environmental samples, researchers currently lack a simple and consistent way to sort large sequence pools into ecologically meaningful categories. We address this issue by introducing FUNGuild, a tool that can be used to taxonomically parse fungal OTUs by ecological guild independent of sequencing platform or analysis pipeline. Using a database and an accompanying bioinformatics script, we demonstrate the application of FUNGuild to three high-throughput sequencing datasets from different habitats: forest soils, grassland soils, and decomposing wood. We found that guilds characteristic of each habitat (i.e., saprotrophic and ectomycorrhizal fungi in forest soils, saprotrophic and arbuscular mycorrhizal fungi in grassland soils, saprotrophic, wood decomposer, and plant pathogenic fungi in decomposing wood) were each well represented. The example datasets demonstrate that while we could quickly and efficiently assign a large portion of the data to guilds, another large portion could not be assigned, reflecting the need to expand and improve the database as well as to gain a better understanding of natural history for many described and undescribed fungal species. As a community resource, FUNGuild is dependent on third-party annotation, so we invite researchers to populate it with new categories and records as well as refine those already in existence.
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Fungi, including symbionts, pathogens and decomposers, play crucial roles in community dynamics and nutrient cycling in terrestrial ecosystems. Despite their ecological importance, the responses of most arctic fungi to climate warming is unknown, so are their potential roles in driving the observed and predicted changes in tundra communities. We carried out deep DNA sequencing of soil samples to study the long-term effects of experimental warming on fungal communities in dry heath and moist tussock tundra in Arctic Alaska. The data presented here indicate that fungal community composition responds strongly to warming in the moist tundra, but not in the dry tundra. While total fungal richness were not significantly affected by warming, there were clear correlations among OTU richness of various ecological and taxonomic groups and long-term warming. Richness of ectomycorrhizal, ericoid mycorrhizal and lichenized fungi generally decreased with warming, while richness of saprotrophic, plant and animal pathogenic, and root endophytic fungi tended to increase in the warmed plots. More importantly, various taxa within these functional guilds followed opposing trends that highlight the importance of species-specific responses to warming. We recommend that species-level ecological differences are taken into account in climate change and nutrient cycling studies that involve arctic fungi. © FEMS 2015. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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Rare taxa overwhelm metabarcoding data generated using next-generation sequencing (NGS). Low frequency Operational Taxonomic Units (OTUs) may be artifacts generated by PCR-amplification errors resulting from polymerase mispairing. We analyzed two Internal Transcribed Spacer 2 (ITS2) MiSeq libraries generated with proofreading (ThermoScientific Phusion®) and non-proofreading (ThermoScientific Phire®) polymerases from the same MiSeq reaction, the same samples, using the same DNA tags, and with two different clustering methods to evaluate the effect of polymerase and clustering tool choices on the estimates of richness, diversity and community composition. Our data show that, while the overall communities are comparable, OTU richness is exaggerated by the use of the non-proofreading polymerase–up to 15 % depending on the clustering method, and on the threshold of low frequency OTU removal. The overestimation of richness also consistently led to underestimation of community evenness, a result of increase in the low frequency OTUs. Stringent thresholds of eliminating the rare reads remedy this issue; exclusion of reads that occurred ≤10 times reduced overestimated OTU numbers to <0.3 %. As a result of these findings, we strongly recommend the use of proofreading polymerases to improve the data integrity as well as the use of stringent culling thresholds for rare sequences to minimize overestimation of community richness.
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Populations near the warm edge of species ranges may be particularly sensitive to climate change, but lack of empirical data on responses to warming represents a key gap in understanding future range dynamics. Herein we document the impacts of experimental warming on the performance of 11 boreal and temperate forest species that co-occur at the ecotone between these biomes in North America. We measured in situ net photosynthetic carbon gain and growth of >4,100 juvenile trees from local seed sources exposed to a chamberless warming experiment that used infrared heat lamps and soil heating cables to elevate temperatures by +3.4 °C above- and belowground for three growing seasons across 48 plots at two sites. In these ecologically realistic field settings, species growing nearest their warm range limit exhibited reductions in net photosynthesis and growth, whereas species near their cold range limit responded positively to warming. Differences among species in their three-year growth responses to warming parallel their photosynthetic responses to warming, suggesting that leaf-level responses may scale to whole-plant performance. These responses are consistent with the hypothesis, from observational data and models, that warming will reduce the competitive ability of currently dominant southern boreal species compared with locally rarer co-occurring species that dominate warmer neighbouring regions.
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Boreal forest soils store a major proportion of the global terrestrial carbon (C) and below-ground inputs contribute as much as above-ground plant litter to the total C stored in the soil. A better understanding of the dynamics and drivers of root-associated fungal communities is essential to predict long-term soil C storage and climate feedbacks in northern ecosystems.We used 454-pyrosequencing to identify fungal communities across fine-scaled soil profiles in a 5000 yr fire-driven boreal forest chronosequence, with the aim of pinpointing shifts in fungal community composition that may underlie variation in below-ground C sequestration.In early successional-stage forests, higher abundance of cord-forming ectomycorrhizal fungi (such as Cortinarius and Suillus species) was linked to rapid turnover of mycelial biomass and necromass, efficient nitrogen (N) mobilization and low C sequestration. In late successional-stage forests, cord formers declined, while ericoid mycorrhizal ascomycetes continued to dominate, potentially facilitating long-term humus build-up through production of melanized hyphae that resist decomposition.Our results suggest that cord-forming ectomycorrhizal fungi and ericoid mycorrhizal fungi play opposing roles in below-ground C storage. We postulate that, by affecting turnover and decomposition of fungal tissues, mycorrhizal fungal identity and growth form are critical determinants of C and N sequestration in boreal forests.
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Arctic regions are experiencing the greatest rates of climate warming on the planet and marked changes have already been observed in terrestrial arctic ecosystems. While most studies have focused on the effects of warming on arctic vegetation and nutrient cycling, little is known about how belowground communities, such as fungi root-associated, respond to warming. Here, we investigate how long-term summer warming affects ectomycorrhizal (ECM) fungal communities. We used Ion Torrent sequencing of the rDNA internal transcribed spacer 2 (ITS2) region to compare ECM fungal communities in plots with and without long-term experimental warming in both dry and moist tussock tundra. Cortinarius was the most OTU-rich genus in the moist tundra, while the most diverse genus in the dry tundra was Tomentella. On the diversity level, in the moist tundra we found significant differences in community composition, and a sharp decrease in the richness of ECM fungi due to warming. On the functional level, our results indicate that warming induces shifts in the extramatrical properties of the communities, where the species with medium-distance exploration type seem to be favored with potential implications for the mobilization of different nutrient pools in the soil. In the dry tundra, neither community richness nor community composition was significantly altered by warming, similar to what had been observed in ECM host plants. There was, however, a marginally significant increase in OTUs identified as ECM fungi with the medium-distance exploration type in the warmed plots. Linking our findings of decreasing richness with previous results of increasing ECM fungal biomass suggests that certain ECM species are favored by warming and may become more abundant, while many other species may go locally extinct due to direct or indirect effects of warming. Such compositional shifts in the community might affect nutrient cycling and soil organic C storage.
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Carbon allocation plays a critical role in forest ecosystem carbon cycling. We reviewed existing literature and compiled annual carbon budgets for forest ecosystems to test a series of hypotheses addressing the patterns, plasticity, and limits of three components of allocation: biomass, the amount of material present; flux, the flow of carbon to a component per unit time; and partitioning, the fraction of gross primary productivity (GPP) used by a component. Can annual carbon flux and partitioning be inferred from biomass? Our survey revealed that biomass was poorly related to carbon flux and to partitioning of photosynthetically derived carbon, and should not be used to infer either. Are component fluxes correlated? Carbon fluxes to foliage, wood, and belowground production and respiration all increased linearly with increasing GPP (a rising tide lifts all boats). Autotrophic respiration was strongly linked to production for foliage, wood and roots, and aboveground net primary productivity and total belowground carbon flux (TBCF) were positively correlated across a broad productivity gradient. How does carbon partitioning respond to variability in resources and environment? Within sites, partitioning to aboveground wood production and TBCF responded to changes in stand age and resource availability, but not to competition (tree density). Increasing resource supply and stand age, with one exception, resulted in increased partitioning to aboveground wood production and decreased partitioning to TBCF. Partitioning to foliage production was much less sensitive to changes in resources and environment. Overall, changes in partitioning within a site in response to resource supply and age were small (
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Rising temperatures are predicted to cause temperate tree species to expand north into currently boreal dominated forests. Other factors, such as overabundant deer, may hinder temperate expansion. We examined how interactions among temperature, browse pressure, light availability, and initial size impact height and radial growth of naturally regenerated, competing temperate and boreal saplings across their overlapping range limits in central North America. In 9 of 10 growth model comparisons, the inclusion of mean summer temperature and browse damage as explanatory variables strongly improved model performance over the base model with only initial size and light availability as parameters. Potential growth reductions due to browse damage and temperature limitation were similar in magnitude (up to ~50%). Temperate sapling growth increased and boreal growth decreased with temperature across a regional summer temperature gradient (2.3 °C), causing a rank reversal in growth rates, and suggesting that temperature is a key driver of sapling performance and range boundaries. However, under high browse pressure positive temperate responses to temperature were eliminated, essentially pushing the crossover point in growth between temperate and boreal species further south. These results highlight the importance of interactions among global change agents and potential impediments for tree species to track a rapidly changing climate.
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Current carbon cycle-climate models predict that future soil carbon storage will be determined by the balance between CO2 fertilization and warming. However, it is uncertain whether greater carbon inputs to soils with elevated CO2 will be sequestered, particularly since warming hastens soil carbon decomposition rates, and may alter the response of soils to new plant inputs. We studied the effects of elevated CO2 and warming on microbial soil carbon decomposition processes using laboratory manipulations of carbon inputs and soil temperature. We incubated soils from the Aspen Free Air CO2 Enrichment experiment, where no accumulation of soil carbon has been observed despite a decade of increased carbon inputs to soils under elevated CO2. We added isotopically-labeled sucrose to these soils in the laboratory to mimic and trace the effects of increased carbon inputs on soil organic carbon decomposition and its temperature sensitivity. Sucrose additions caused a positive priming of soil organic carbon decomposition, demonstrated by increased respiration derived from soil carbon, increased microbial abundance, and a shift in the microbial community towards faster growing microorganisms. Similar patterns were observed for elevated CO2 soils, suggesting that the priming effect was responsible for reductions in soil carbon accumulation at the site. Laboratory warming accelerated the rate of the priming effect, but the magnitude of the priming effect was not different amongst temperatures, suggesting that the priming effect was limited by substrate availability, not soil temperature. No changes in substrate use efficiency were observed with elevated CO2 or warming. The stimulatory effects of warming on the priming effect suggest that increased belowground carbon inputs from CO2 fertilization are not likely to be stored in mineral soils.
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