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Defending Earth’s terrestrial microbiome
Abstract
Microbial life represents the majority of Earth’s biodiversity. Across disparate disciplines from medicine to forestry, scientists continue to discover how the microbiome drives essential, macro-scale processes in plants, animals and entire ecosystems. Yet, there is an emerging realization that Earth’s microbial biodiversity is under threat. Here we advocate for the conservation and restoration of soil microbial life, as well as active incorporation of microbial biodiversity into managed food and forest landscapes, with an emphasis on soil fungi. We analyse 80 experiments to show that native soil microbiome restoration can accelerate plant biomass production by 64% on average, across ecosystems. Enormous potential also exists within managed landscapes, as agriculture and forestry are the dominant uses of land on Earth. Along with improving and stabilizing yields, enhancing microbial biodiversity in managed landscapes is a critical and underappreciated opportunity to build reservoirs, rather than deserts, of microbial life across our planet. As markets emerge to engineer the ecosystem microbiome, we can avert the mistakes of aboveground ecosystem management and avoid microbial monocultures of single high-performing microbial strains, which can exacerbate ecosystem vulnerability to pathogens and extreme events. Harnessing the planet’s breadth of microbial life has the potential to transform ecosystem management, but it requires that we understand how to monitor and conserve the Earth’s microbiome. Efforts to futureproof global microbial biodiversity are proposed, in particular in managed landscapes, to monitor, manage and restore the soil fungal microbiome.
... Averill et al. [6] employed meta-analysis from eighty different studies to demonstrate that enriching the soil with advantageous microbes can dramatically increase the size of plants. Moreover, nanofertilizers have been discussed to alter soil conditions and microbiome stability to enhance plant productivity [7][8]. ...
The sustainability of plant life is intimately connected to its evolution with microbial life. Based on experimental evidence, microbial assemblages benefit plants on molecular, cellular, and ecological levels. The plant microbiome or phytomicrobiome are the microbes closely associated with a particular plant species. Distinct plant microbial ecosystems are in the phyllosphere, rhizosphere, soil, and endosphere. Plant-associated microbes affect plants in numerous ways and participate in various physiological functions essential for the plant, including nutrient recycling, the breakdown and synthesis of critical molecules, and other phytoprotective functions. While studying plant-microbe interactions is not new, recent developments in metagenomic sequencing and high-throughput pathway identification techniques have allowed scientists to explore unculturable microbes associated with plants. This review primarily focuses on the significant role of the phytomicrobiome and describes the prevalent taxonomic units found in association with plants. Plants are suitable tractable model systems to study plant-microbe interactions and can be grown under different experimental conditions to examine other characteristics of the phytomicrobiome. This article also provides a systematic review of the current research on the phytomicrobiome. It explores the extent to which the phytomicrobiome participates in an essential process that promotes plant fitness and sustainabilityand reviews research that focuses on microbiome community shifts in response to abiotic and biotic stress. Genetic engineering of plant-associated microbes to enhance plant growth and protection is addressed. The use of nanofertilizers and phytomicrobiome transplantation to restore plant health and improve the success of agriculturally beneficial crops is also discussed.
... In this context, and given all the above considerations, we need to conserve the existing microbial biodiversity of healthy ecosystems, especially in drylands, because it is the "key to soil survival". Furthermore, it is pivotal to incorporate the microbial component into the ecosystem restoration planning to rebuild the disturbed ecosystem microbiome and take it into account within the land management practices (Averill et al., 2022). ...
Our planet teeters on the brink of massive ecosystem collapses, and arid regions experience manifold environmental and climatic challenges that increase the magnitude of selective pressures on already stressed ecosystems. Ultimately, this leads to their aridification and desertification, that is, to simplified and barren ecosystems (with proportionally less microbial load and diversity) with altered functions and food webs and modification of microbial community network. Thus, preserving and restoring soil health in such a fragile biome could help buffer climate change's effects. We argue that microorganisms and the protection of their functional properties and networks are key to fight desertification. Specifically, we claim that it is rational, possible and certainly practical to rely on native dryland edaphic microorganisms and microbial communities as well as dryland plants and their associated microbiota to conserve and restore soil health and mitigate soil depletion in newly aridified lands. Furthermore, this will meet the objective of protecting/stabilizing (and even enhancing) soil biodiversity globally. Without urgent conservation and restoration actions that take into account microbial diversity, we will ultimately, and simply, not have anything to protect anymore. By considering recent literature, we discuss how dryland microorganisms could notably be used in the protection of the soil and, in general, the dryland environment and improve world food production. More specifically, we expose our vision on why and how drylands—among the most dominant terrestrial biome surface‐wise—are expanding under the threat of climate change, and their indigenous microbiota could be used (i) to design desertification mitigation strategies and (ii) to improve dryland agriculture.
... Although a warming experiment will not mimic the historical conditions experienced by locally extinct species during their decline, it can reveal whether a specific threat (here, warminginduced changes in PSF) is associated with decreased performance in locally extinct species, potentially leading to the development of successful reintroduction or management strategies where these species persist (Caughlin et al. 2019). This empirical approach can also address whether warming-induced changes in soil biota represent a contemporary threat to extant species and should be considered in conservation efforts (Averill et al. 2022). ...
PurposeClimate change may alter interactions between plants and their associated soil microbial communities, including microbe-mediated plant-soil feedbacks (PSF). If PSF influence plant performance and abundance in natural communities, climate-induced changes in soil communities might affect local extinction. Here, we examine whether warming-induced shifts in plant-soil interactions are associated with local species loss in tallgrass prairie.Methods
We conducted a traditional two-phase PSF experiment. In phase 1, phylogenetic pairs of locally extinct and extant prairie species were grown under ambient or elevated temperature conditions in the field. In phase 2, soil microbial communities were collected from below those plants and inoculated onto conspecific and heterospecific seedlings grown in the greenhouse. We compared warming effects on plant performance in soil conditioned by locally extinct and extant species as well as net-pairwise PSF between phylogenetic pairs.ResultsLocally extinct prairie species were more sensitive to soil biota than extant species, generally performing better when grown in soils cultivated by certain extant species. Meanwhile, extant species were more responsive to warming effects on soil communities than locally extinct species, although the direction and magnitude of temperature effects varied across species. We detected no significant overall effects of warming on net-pairwise PSF.Conclusion
These findings suggest that soil biota might have affected historical plant species losses via negative effects of locally extinct species’ soil on their own growth. Warming-induced shifts in soil communities might influence extant prairie species’ performance under climate change, indicating a need to consider plant–microbe interactions in future prairie conservation efforts.
... In this era of rapid industrialization, discharge of numerous hazardous effluents from industries into fresh water bodies is increasingly destroying biodiversity (Sarkar et al. 2017;Averill et al. 2022). Industrial pollution is also one of the main causes of thermal pollution, which increases water temperatures and decreases dissolved oxygen concentrations. ...
In an era of rapid industrialization, the discharge of contaminated effluent into natural environments has significantly increased with a direct, negative impact on aquatic biodiversity. It is not only discharged industrial effluent, but also products discharged from wastewater treatment plants, that disrupt biogeochemical cycles, which have direct relationships with aquatic biodiversity. Due to this situation, microbial biodiversity is also affected. Microbial wastewater treatment is a sustainable way to protect aquatic biodiversity, for which environmental microbiome conservation is very important. This article explores the delicate topic of biodiversity conservation, specifically aquatic biodiversity conservation, and is aimed at improving and informing aquatic biodiversity policies.
KEY POLICY INSIGHTS • In this time of fast industrialization, microbial biodiversity in the aquatic world is getting impacted due to wastewater effluents. • Designing and revising the policies/laws required to conserve microbial biodiversity for the sustainability of our planet via bioregional management, and public awareness programmes. • Microbiome conservation will play a key role in maintaining the global aquatic biome, which is at ecological risk.
Forests influence climate and mitigate global change through the storage of carbon in soils. In turn, these complex ecosystems face important challenges, including increases in carbon dioxide, warming, drought and fire, pest outbreaks and nitrogen deposition. The response of forests to these changes is largely mediated by microorganisms, especially fungi and bacteria. The effects of global change differ among boreal, temperate and tropical forests. The future of forests depends mostly on the performance and balance of fungal symbiotic guilds, saprotrophic fungi and bacteria, and fungal plant pathogens. Drought severely weakens forest resilience, as it triggers adverse processes such as pathogen outbreaks and fires that impact the microbial and forest performance for carbon storage and nutrient turnover. Nitrogen deposition also substantially affects forest microbial processes, with a pronounced effect in the temperate zone. Considering plant-microorganism interactions would help predict the future of forests and identify management strategies to increase ecosystem stability and alleviate climate change effects. In this Review, we describe the impact of global change on the forest ecosystem and its microbiome across different climatic zones. We propose potential approaches to control the adverse effects of global change on forest stability, and present future research directions to understand the changes ahead.
Grazing by large mammalian herbivores impacts climate as it can favor the size and stability of a large carbon (C) pool in the soils of grazing ecosystems. As native herbivores in the world's grasslands, steppes, and savannas are progressively being displaced by livestock, it is important to ask whether livestock can emulate the functional roles of their native counterparts. While livestock and native herbivores can have remarkable similarity in their traits, they can differ greatly in their impacts on vegetation composition which can affect soil-C. It is uncertain how these similarities and differences impact soil-C via their influence on microbial decomposers. We test competing alternative hypotheses with a replicated, long-term, landscape-level, grazing-exclusion experiment to ask whether livestock in the Trans-Himalayan ecosystem of northern India can match decadal-scale (2005-2016) soil-C stocks under native herbivores. We evaluate multiple lines of evidence from 17 variables that influence soil-C (quantity and quality of C-input from plants, microbial biomass and metabolism, microbial community composition, eDNA, veterinary antibiotics in soil), and assess their inter-relationships. Livestock and native herbivores differed in their effects on several soil microbial processes. Microbial carbon use efficiency (CUE) was 19% lower in soils under livestock. Compared to native herbivores, areas used by livestock contained 1.5 kg C m-2 less soil-C. Structural equation models showed that alongside the effects arising from plants, livestock alter soil microbial communities which is detrimental for CUE, and ultimately also for soil-C. Supporting evidence pointed toward a link between veterinary antibiotics used on livestock, microbial communities, and soil-C. Overcoming the challenges of sequestering antibiotics to minimize their potential impacts on climate, alongside microbial rewilding under livestock, may reconcile the conflicting demands from food-security and ecosystem services. Conservation of native herbivores and alternative management of livestock is crucial for soil-C stewardship to envision and achieve natural climate solutions.
Environmental microbiome engineering is emerging as a potential avenue for climate change mitigation. In this process, microbial inocula are introduced to natural microbial communities to tune activities that regulate the long-term stabilization of carbon in ecosystems. In this review, we outline the process of environmental engineering and synthesize key considerations about ecosystem functions to target, means of sourcing microorganisms, strategies for designing microbial inocula, methods to deliver inocula, and the factors that enable inocula to establish within a resident community and modify an ecosystem function target. Recent work, enabled by high-throughput technologies and modeling approaches, indicate that microbial inocula designed from the top down, particularly through directed evolution, may generally have a higher chance of establishing within existing microbial communities than other historical approaches to microbiome engineering. We address outstanding questions about the determinants of inocula establishment and provide suggestions for further research about the possibilities and challenges of environmental microbiome engineering as a tool to combat climate change.
The immense diversity and biomass of ericoid-, ectomycorrhizal, and saprotrophic fungal guilds in boreal forest soils make them vital components of conservation and ecosystem processes, and in particular, many ectomycorrhizal fungi are considered species of conservation concern. However, amalgamated information on the functions and relationships of soil fungi to perceived forest conservation values, and how inter and intra-guild interactions affect the accretion and decomposition of soil organic matter is lacking. In a long-term factorial shrub removal and pine root exclusion experiment, I assessed guild contributions to soil respiration and decomposition of organic substrates guided by ecological theory. Then in the northern and southern boreal forest, I evaluated whether forest conservation values are aligned with the diversity of ectomycorrhizal fungi. Overall, the ericoid guild makes a significant contribution to total soil respiration (11 ± 9%), and ericoid activities appeared to be more sensitive to periods of drought compared to ectomycorrhizal (43 ± 1%) and saprotrophic (53 ± 5%) guilds. Saprotrophic-ectomycorrhizal interactions during decomposition led to a modest, yet inconsistent Gadgil effect (10%) for early-stage litter decomposition. Ericoid and ectomycorrhizal guilds interactions were determined to be more important for late-stage organic matter balance in boreal forest soils. Ectomycorrhizal species richness was significantly higher in the southern boreal forest compared to the north. Furthermore, forest conservation values across the boreal forest were not adequately related to ectomycorrhizal diversity through DNA-metabarcoding. Instead, soil fertility, corresponding to tree species basal area, was the clearest indicator of ectomycorrhizal diversity and composition in both regions. Mycorrhizal guilds may be underappreciated and understudied in terms of conservation, but their functional roles in the accumulation and decomposition of organic matter in long-term soil carbon pools emphasizes the importance of evaluating the many dimensions of fungal conservation in boreal forests.
Global biodiversity loss and mass extinction of species are two of the most critical environmental issues the world is currently facing, resulting in the disruption of various ecosystems central to environmental functions and human health. Microbiome-targeted interventions, such as probiotics and microbiome transplants, are emerging as potential options to reverse deterioration of biodiversity and increase the resilience of wildlife and ecosystems. However, the implementation of these interventions is urgently needed. We summarize the current concepts, bottlenecks and ethical aspects encompassing the careful and responsible management of ecosystem resources using the microbiome (termed microbiome stewardship) to rehabilitate organisms and ecosystem functions. We propose a real-world application framework to guide environmental and wildlife probiotic applications. This framework details steps that must be taken in the upscaling process while weighing risks against the high toll of inaction. In doing so, we draw parallels with other aspects of contemporary science moving swiftly in the face of urgent global challenges. Careful and responsible microbiome management is a critical strategy to counter biodiversity loss, but practical and regulatory hurdles must be addressed to maximize its utility.
Mega‐fires of unprecedented size, intensity, and socio‐economic impacts have surged globally due to climate change, fire suppression, and development. Soil microbiomes are critical for post‐fire plant regeneration and nutrient cycling, yet how mega‐fires impact the soil microbiome remains unclear. We had a serendipitous opportunity to obtain pre‐ and post‐fire soils from the same sampling locations after the 2016 Soberanes mega‐fire burned with high severity throughout several of our established redwood‐tanoak plots. This makes our study the first to examine microbial fire response in redwood‐tanoak forests. We re‐sampled soils immediately post‐fire from two burned plots and one unburned plot to elucidate the effect of mega‐fire on soil microbiomes. We used Illumina MiSeq sequencing of 16S and ITS1 to determine that bacterial and fungal richness were reduced by 38‐70% in burned plots, with richness unchanged in the unburned plot. Fire altered composition by 27% for bacteria and 24% for fungi, whereas the unburned plots experienced no change in fungal and negligible change in bacterial composition. We observed pyrophilous taxa that positively responded to fire were phylogenetically conserved, suggesting shared evolutionary traits. For bacteria, fire selected for increased Firmicutes and Actinobacteria. For fungi, fire selected for the Ascomycota classes Pezizomycetes and Eurotiomycetes and for a Basidiomycota class of heat‐resistant Geminibasidiomycete yeasts. We build from Grime’s Competitor‐Stress tolerator‐Ruderal (C‐S‐R) framework and its recent microbial applications to show how our results might fit into a trait‐based conceptual model to help predict generalizable microbial responses to fire.
Most trees form symbioses with ectomycorrhizal fungi (EMF) which influence access to growth-limiting soil resources. Mesocosm experiments repeatedly show that EMF species differentially affect plant development, yet whether these effects ripple up to influence the growth of entire forests remains unknown. Here we tested the effects of EMF composition and functional genes relative to variation in well-known drivers of tree growth by combining paired molecular EMF surveys with high-resolution forest inventory data across 15 European countries. We show that EMF composition was linked to a threefold difference in tree growth rate even when controlling for the primary abiotic drivers of tree growth. Fast tree growth was associated with EMF communities harboring high inorganic but low organic nitrogen acquisition gene proportions and EMF which form contact versus medium-distance fringe exploration types. These findings suggest that EMF composition is a strong bio-indicator of underlying drivers of tree growth and/or that variation of forest EMF communities causes differences in tree growth. While it may be too early to assign causality or directionality, our study is one of the first to link fine-scale variation within a key component of the forest microbiome to ecosystem functioning at a continental scale. The ISME Journal; https://doi.
There is a global industry built upon the production of “bioinoculants,” which include both bacteria and fungi. The recent increase in bioinoculant uptake by land users coincides with a drive for more sustainable land use practices. But are bioinoculants sustainable? These microbes are believed to improve plant performance, but knowledge of their effect on resident microbial communities is scant. Without a clear understanding of how they affect soil microbial communities (SMC), their utility is unclear. To assess how different inoculation practices may affect bioinoculant effects on SMC, we surveyed the existing literature. Our results show that bioinoculants significantly affect soil microbial diversity and that these effects are mediated by inoculant type, diversity, and disturbance regime. Further, these changes to soil microbes affect plant outcomes. Knowledge that these products may influence crop performance indirectly through changes to soil microbial diversity attests to the importance of considering the soil microbiome when assessing both bioinoculant efficacy and threats to soil ecosystems.
Many countries have adopted large-scale tree planting programmes as a climate mitigation strategy and to support local livelihoods. We evaluate a series of large-scale tree planting programmes using data collected from historical Landsat imagery in the state of Himachal Pradesh in Northern India. Using this panel dataset, we use an event study design to estimate the socioeconomic and biophysical impacts over decades of these programmes. We find that tree plantings have not, on average, increased the proportion of forest canopy cover and have modestly shifted forest composition away from the broadleaf varieties valued by local people. Further cross-sectional analysis, from a household livelihood survey, shows that tree planting supports little direct use by local people. We conclude that decades of expensive tree planting programmes in this region have not proved effective. This result suggests that large-scale tree planting may sometimes fail to achieve its climate mitigation and livelihood goals. Large-scale tree planting programmes have been implemented or planned for areas around the world suffering from deforestation, but this study presents evidence that such efforts may not necessarily deliver the desired environmental and economic outcomes.
Recent reports indicate that the health of our planet is getting worse and that genuine transformative changes are pressing. So far, efforts to ameliorate Earth's ecosystem crises have been insufficient, as these often depart from current knowledge of the underlying ecological processes. Nowadays, biodiversity loss and the alterations in biogeochemical cycles are reaching thresholds that put the survival of our species at risk. Biological interactions are fundamental for achieving biological conservation and restoration of ecological processes, especially those that contribute to nutrient cycles. Microorganism are recognized as key players in ecological interactions and nutrient cycling, both free-living and in symbiotic associations with multicellular organisms. This latter assemblage work as a functional ecological unit called "holobiont." Here, we review the emergent ecosystem properties derived from holobionts, with special emphasis on detritivorous terrestrial arthropods and their symbiotic microorganisms. We revisit their relevance in the cycling of recalcitrant organic compounds (e.g., lignin and cellulose). Finally, based on the interconnection between biodiversity and nutrient cycling, we propose that a multicellular organism and its associates constitute an Ecosystem Holobiont (EH). This EH is the functional unit characterized by carrying out key ecosystem processes. We emphasize that in order to meet the challenge to restore the health of our planet it is critical to reduce anthropic pressures that may threaten not only individual entities (known as "bionts") but also the stability of the associations that give rise to EH and their ecological functions.
The interest in the use of microorganisms in agricultural practices has increased significantly in recent years, both in the promotion of plant growth and in the biological control of plant pests and diseases. This literature review work aimed to address information on the use of isolation, multiplication, use and storage methodologies for efficient microorganisms (Effective Microorganisms, EM) in agriculture. These microorganisms have important functions for their hosts, as they have symbiotic interactions with them, and are capable of protecting plants from attack by insects, diseases and herbivorous mammals through the production of toxins. The use of EM in agriculture aims to accelerate the natural composition of organic matter and promote the balance of microbial flora contributing to plant development. EMs are potential substitutes for chemical products, and can thus favor the preservation of the environment. They are collected from fertile forest soils through simple and inexpensive methodologies, consisting of a tool with potential to be used both by family farmers and on a small and large scale. They can be used in different ways, the main ones being in soil, plant, water and animals. The use of EM is an accessible and low-cost technique, in addition to being easy to prepare within the property itself, contributing to the sustainability of agricultural systems.
Aim
Soil microbes are essential for maintenance of life‐supporting ecosystem services, but projections of how these microbes will be affected by global change scenarios are lacking. Therefore, our aim was to provide projections of future soil microbial distribution using several scenarios of global change.
Location
Global.
Time period
1950–2090.
Major taxa studied
Bacteria and fungi.
Methods
We used a global database of soil microbial communities across six continents to estimate past and future trends of the soil microbiome. To do so, we used structural equation models to include the direct and indirect effects of changes in climate and land use in our predictions, using current climate (temperature and precipitation) and land‐use projections between 1950 and 2090.
Results
Local bacterial richness will increase in all scenarios of change in climate and land use considered, although this increase will be followed by a generalized community homogenization process affecting > 85% of terrestrial ecosystems. Changes in the relative abundance of functional genes associated with the increases in bacterial richness are also expected. Based on an ecological cluster analysis, our results suggest that phylotypes such as Geodermatophilus spp. (typical desert bacteria), Mycobacterium sp. (which are known to include important human pathogens), Streptomyces mirabilis (major producers of antibiotic resistance genes) or potential fungal soil‐borne plant pathogens belonging to Ascomycota fungi (Venturia spp., Devriesia spp.) will become more abundant in their communities.
Main conclusions
Our results provide evidence that climate change has a stronger influence on soil microbial communities than change in land use (often including deforestation and agricultural expansion), although most of the effects of climate are indirect, through other environmental variables (e.g., changes in soil pH). The same was found for microbial functions such as the prevalence of phosphate transport genes. We provide reliable predictions about the changes in the global distribution of microbial communities, showing an increase in alpha diversity and a homogenization of soil microbial communities in the Anthropocene.
The arbuscular mycorrhizal (AM) fungi are a globally‐distributed group of soil organisms that play critical roles in ecosystem function. However, the ecological niches of individual AM fungal taxa are poorly understood. We collected >300 soil samples from natural ecosystems worldwide and modelled the realized niches of AM fungal virtual taxa (VT; approximately species‐level phylogroups). We found that environmental and spatial variables jointly explained VT distribution worldwide, with temperature and pH being the most important abiotic drivers, and spatial effects generally occurring at local‐ to regional‐scales. While dispersal limitation could explain some variation in VT distribution, VT relative abundance was almost exclusively driven by environmental variables. Several environmental and spatial effects on VT distribution and relative abundance were correlated with phylogeny, indicating that closely related VT exhibit similar niche optima and widths. Major clades within Glomeraceae exhibited distinct niche optima, Acaulosporaceae generally had niche optima in low pH and low temperature conditions, and Gigasporaceae generally had niche optima in high precipitation conditions. Identifying the realized niche space occupied by individual and phylogenetic groups of soil microbial taxa provides a basis for building detailed hypotheses about how soil communities respond to gradients and manipulation in ecosystems worldwide.
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.
While the importance of mutualisms across the tree of life is recognized, it
is not understood why some organisms evolve high levels of dependence on
mutualistic partnerships, while other species remain autonomous or retain
or regain minimal dependence on partners.We identify four main pathways
leading to the evolution of mutualistic dependence. Then, we evaluate current
evidence for three predictions: (a) Mutualisms with different levels of
dependence have distinct stabilizing mechanisms against exploitation and
cheating, (b) less dependent mutualists will return to autonomy more often
than those that are highly dependent, and (c) obligate mutualisms should
be less context dependent than facultative ones. Although we find evidence
supporting all three predictions, we stress that mutualistic partners follow
diverse paths toward—and away from—dependence.We also highlight the
need to better examine asymmetry in partner dependence. Recognizing how
variation in dependence influences the stability, breakdown, and context dependence
of mutualisms generates new hypotheses regarding how and why
the benefits of mutualistic partnerships differ over time and space.
More than half of all tropical forests are degraded by human impacts, leaving them threatened with conversion to agricultural plantations and risking substantial biodiversity and carbon losses. Restoration could accelerate recovery of aboveground carbon density (ACD), but adoption of restoration is constrained by cost and uncertainties over effectiveness. We report a long-term comparison of ACD recovery rates between naturally regenerating and actively restored logged tropical forests. Restoration enhanced decadal ACD recovery by more than 50%, from 2.9 to 4.4 megagrams per hectare per year. This magnitude of response, coupled with modal values of restoration costs globally, would require higher carbon prices to justify investment in restoration. However, carbon prices required to fulfill the 2016 Paris climate agreement [$40 to $80 (USD) per tonne carbon dioxide equivalent] would provide an economic justification for tropical forest restoration.
Temperate and boreal forests are increasingly suffering from anthropic degradation. Ectomycorrhizal fungi (EMF) are symbionts with most temperate and boreal forest trees, providing their hosts with soil nutrients and water in exchange for plant carbon. This group of fungi is involved in woody plants' survival and growth and helps plants tolerate harsh environmental conditions. Here, we describe the current understanding of how EMF can benefit temperate and boreal forest restoration projects. We review current evidence on promising restoration plans that actively use EMF in sites contaminated with heavy metals, affected by soil erosion, and degraded due to clearcut logging and wildfire. We discuss the potential role of this group of fungi for restoring sites invaded by non-native plant species. Additionally, we explore limitations, knowledge gaps, and possible undesired outcomes of the use of EMF in forest restoration, and we suggest how to further incorporate this fungal group into forest management. We conclude that considering EMF-host interactions could improve the chances of success of future restoration programs in boreal and temperate forests.
Soils harbor a substantial fraction of the world’s biodiversity, contributing to many crucial ecosystem functions. It is thus essential to identify general macroecological patterns related to the distribution and functioning of soil organisms to support their conservation and consideration by governance. These macroecological analyses need to represent the diversity of environmental conditions that can be found worldwide. Here we identify and characterize existing environmental gaps in soil taxa and ecosystem functioning data across soil macroecological studies and 17,186 sampling sites across the globe. These data gaps include important spatial, environmental, taxonomic, and functional gaps, and an almost complete absence of temporally explicit data. We also identify the limitations of soil macroecological studies to explore general patterns in soil biodiversity-ecosystem functioning relationships, with only 0.3% of all sampling sites having both information about biodiversity and function, although with different taxonomic groups and functions at each site. Based on this information, we provide clear priorities to support and expand soil macroecological research. Soil organism biodiversity contributes to ecosystem function, but biodiversity and function have not been equivalently studied across the globe. Here the authors identify locations, environment types, and taxonomic groups for which there is currently a lack of biodiversity and ecosystem function data in the existing literature.
Introductions and invasions by fungi, especially pathogens and mycorrhizal fungi, are widespread and potentially highly consequential for native ecosystems, but may also offer opportunities for linking microbial traits to their ecosystem functions. In particular, treating ectomycorrhizal (EM) invasions, i.e., co-invasions by EM fungi and their EM host plants, as natural experiments may offer a powerful approach for testing how microbial traits influence ecosystem functions. Forests dominated by EM symbiosis have unique biogeochemistry whereby the secretions of EM plants and fungi affect carbon (C) and nutrient cycling; moreover, particular lineages of EM fungi have unique functional traits. EM invasions may therefore alter the biogeochemistry of the native ecosystems they invade, especially nitrogen (N) and C cycling. By identifying “response traits” that favor the success of fungi in introductions and invasions (e.g., spore dispersal and germination) and their correlations with “effect traits” (e.g., nutrient-cycling enzymes) that can alter N and C cycling (and affect other coupled elemental cycles), one may be able to predict the functional consequences for ecosystems of fungal invasions using biogeochemistry models that incorporate fungal traits. Here, we review what is already known about how EM fungal community composition, traits, and ecosystem functions differ between native and exotic populations, focusing on the example of EM fungi associated with species of Pinus introduced from the Northern into the Southern Hemisphere. We develop hypotheses on how effects of introduced and invasive EM fungi may depend on interactions between soil N availability in the exotic range and EM fungal traits. We discuss how such hypotheses could be tested by utilizing Pinus introductions and invasions as a model system, especially when combined with controlled laboratory experiments. Finally, we illustrate how ecosystem modeling can be used to link fungal traits to their consequences for ecosystem N and C cycling in the context of biological invasions, and we highlight exciting avenues for future directions in understanding EM invasion.
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.
Biodiversity on the Earth is changing at an unprecedented rate due to a variety of global change factors (GCFs). However, the effects of GCFs on microbial diversity is unclear despite that soil microorganisms play a critical role in biogeochemical cycling. Here, we synthesize 1235 GCF observations worldwide and show that microbial rare species are more sensitive to GCFs than common species, while GCFs do not always lead to a reduction in microbial diversity. GCFs-induced shifts in microbial alpha diversity can be predominately explained by the changed soil pH. In addition, GCF impacts on soil functionality are explained by microbial community structure and biomass rather than the alpha diversity. Altogether, our findings of GCF impacts on microbial diversity are fundamentally different from previous knowledge for well-studied plant and animal communities, and are crucial to policy-making for the conservation of microbial diversity hotspots under global changes. It is often assumed that various types of anthropogenic change reduce microbial diversity and function. Here, the authors do a meta-analysis showing that global change factors affect microbial diversity inconsistently; negative effects are most likely for global change factors that affect soil pH.
Theory and observation for the search for life on exoplanets via atmospheric ‘biosignature gases’ is accelerating, motivated by the capabilities of the next generation of space- and ground-based telescopes. The most observationally accessible rocky planet atmospheres are those dominated by molecular hydrogen gas, because the low density of H2 gas leads to an expansive atmosphere. The capability of life to withstand such exotic environments, however, has not been tested in this context. We demonstrate that single-celled microorganisms (Escherichia coli and yeast) that normally do not inhabit H2-dominated environments can survive and grow in a 100% H2 atmosphere. We also describe the astonishing diversity of dozens of different gases produced by E. coli, including many already proposed as potential biosignature gases (for example, nitrous oxide, ammonia, methanethiol, dimethylsulfide, carbonyl sulfide and isoprene). This work demonstrates the utility of laboratory experiments to better identify which kinds of alien environments can host some form of possibly detectable life. Escherichia coli bacteria and yeast cultures (representative prokaryotes and eukaryotes) have been tested under laboratory conditions in a 100% H2 atmosphere. They can reproduce normally, with lower growth rates, producing a range of biosignature gases. Exoplanets with a H2-dominated atmosphere might thus not be totally hostile to some forms of life.
Ecological restoration is practiced worldwide as a direct response to the degradation and destruction of ecosystems. In addition to its ecological impact it has enormous potential to improve population health, socio‐economic wellbeing, and the integrity of diverse national and ethnic cultures. In recognition of the critical role of restoration in ecosystem health, the United Nations declared 2021–2030 as the Decade on Ecosystem Restoration. We propose six practical strategies to strengthen the effectiveness and amplify the work of ecological restoration to meet the aspirations of the Decade: (1) incorporate holistic actions, including working at effective scale; (2) include Traditional Ecological Knowledge (TEK); (3) collaborate with allied movements and organizations; (4) advance and apply soil microbiome science and technology; (5) study and show the relationships between ecosystem health and human health; and (6) provide training and capacity‐building opportunities for communities and practitioners. We offer these in the hope of identifying possible leverage points and pathways for collaborative action among interdisciplinary groups already committed to act and support the UN Decade on Ecosystem Restoration. Collectively, these six strategies work synergistically to improve human health and also the health of the ecosystems on which we all depend, and can be the basis for a global restorative culture.
This article is protected by copyright. All rights reserved.
Organismal biology has undergone a dramatic paradigm shift in the last decade. The realization that host cells and genes are outnumbered by symbiotic microbial cells and their genes has forced us to rethink our focus on ‘individuals’. It is also becoming increasingly clear that the ecology and biology of animals and plants are intimately connected with their microbial partners. In the context of conserving functioning species, such revelatory insights beg the question—what exactly should we be trying to conserve? Here, we review how an understanding of host–microbe interactions can benefit conservation biology. We propose a way forward for conservation biologists, to gather evidence of the potential effects of changes to plant and animal microbiomes, and to incorporate the holobiont concept into applied conservation practice. In humans, microbes influence physiology, health, behaviour and psychology. In animals and plants, microbes similarly influence critically important components of health, communication and (in animals) behaviour. Together, the animal or plant and all of its associated micro‐organisms are termed the holobiont. At the same time, humans are now the strongest evolutionary force on the planet, causing global change at unprecedented scale. We know that microbial diversity in humans has been compromised in urban societies, with a growing list of consequences for health and function. While we still have limited evidence for similar effects in plants and animals, anthropogenic factors that affect diversity are also likely to affect animal and plant microbiomes, with similar associated effects on host function and health. Microbiome research is still in its relative infancy, particularly in its application to plants and animals, yet the tools are becoming more widely available and affordable. Forward‐looking conservation biologists could harness such tools and apply them to the study of plant and animal microbiomes with the goal of understanding which microbiota might be required to ensure future viability of conserved host populations. For now, the precautionary principle applies. We suggest that, to meaningfully and effectively conserve a species, we must also consider how to conserve the bacteria, viruses, fungi and other symbionts intimately associated with that macro‐organism. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.
Microbes' role in soil decomposition
Soils harbor a rich diversity of invertebrate and microbial life, which drives biogeochemical processes from local to global scales. Relating the biodiversity patterns of soil ecological communities to soil biogeochemistry remains an important challenge for ecologists and earth system modelers. Crowther et al. review the state of science relating soil organisms to biogeochemical processes, focusing particularly on the importance of microbial community variation on decomposition and turnover of soil organic matter. Although there is variation in soil communities across the globe, ecologists are beginning to identify general patterns that may contribute to predicting biogeochemical dynamics under future climate change.
Science , this issue p. eaav0550
Despite having key functions in terrestrial ecosystems, information on the dominant soil fungi and their ecological preferences at the global scale is lacking. To fill this knowledge gap, we surveyed 235 soils from across the globe. Our findings indicate that 83 phylotypes (<0.1% of the retrieved fungi), mostly belonging to wind dispersed, generalist Ascomycota, dominate soils globally. We identify patterns and ecological drivers of dominant soil fungal taxa occurrence, and present a map of their distribution in soils worldwide. Whole-genome comparisons with less dominant, generalist fungi point at a significantly higher number of genes related to stress-tolerance and resource uptake in the dominant fungi, suggesting that they might be better in colonising a wide range of environments. Our findings constitute a major advance in our understanding of the ecology of fungi, and have implications for the development of strategies to preserve them and the ecosystem functions they provide.
Recent demonstrations of the role of plant–soil biota interactions have challenged the conventional view that vegetation changes are mainly driven by changing abiotic conditions. However, while this concept has been validated under natural conditions, our understanding of the long‐term consequences of plant–soil interactions for above‐belowground community assembly is restricted to mathematical and conceptual model projections. Here, we demonstrate experimentally that one‐time additions of soil biota and plant seeds alter soil‐borne nematode and plant community composition in semi‐natural grassland for 20 years. Over time, aboveground and belowground community composition became increasingly correlated, suggesting an increasing connectedness of soil biota and plants. We conclude that the initial composition of not only plant communities, but also soil communities has a long‐lasting impact on the trajectory of community assembly.
The Global Deal for Nature (GDN) is a time-bound, science-driven plan to save the diversity and abundance of life on Earth. Pairing the GDN and the Paris Climate Agreement would avoid catastrophic climate change, conserve species, and secure essential ecosystem services. New findings give urgency to this union: Less than half of the terrestrial realm is intact, yet conserving all native ecosystems—coupled with energy transition measures—will be required to remain below a 1.5°C rise in average global temperature. The GDN targets 30% of Earth to be formally protected and an additional 20% designated as climate stabilization areas, by 2030, to stay below 1.5°C. We highlight the 67% of terrestrial ecoregions that can meet 30% protection, thereby reducing extinction threats and carbon emissions from natural reservoirs. Freshwater and marine targets included here extend the GDN to all realms and provide a pathway to ensuring a more livable biosphere.
Root-associated microbes play a key role in plant performance and productivity, making them important players in agroecosystems. So far, very few studies have assessed the impact of different farming systems on the root microbiota and it is still unclear whether agricultural intensification influences the structure and complexity of microbial communities. We investigated the impact of conventional, no-till, and organic farming on wheat root fungal communities using PacBio SMRT sequencing on samples collected from 60 farmlands in Switzerland. Organic farming harbored a much more complex fungal network with significantly higher connectivity than conventional and no-till farming systems. The abundance of keystone taxa was the highest under organic farming where agricultural intensification was the lowest. We also found a strong negative association (R2 = 0.366; P < 0.0001) between agricultural intensification and root fungal network connectivity. The occurrence of keystone taxa was best explained by soil phosphorus levels, bulk density, pH, and mycorrhizal colonization. The majority of keystone taxa are known to form arbuscular mycorrhizal associations with plants and belong to the orders Glomerales, Paraglomerales, and Diversisporales. Supporting this, the abundance of mycorrhizal fungi in roots and soils was also significantly higher under organic farming. To our knowledge, this is the first study to report mycorrhizal keystone taxa for agroecosystems, and we demonstrate that agricultural intensification reduces network complexity and the abundance of keystone taxa in the root microbiome.
A substantial body of evidence has demonstrated that biodiversity stabilizes ecosystem functioning over time in grassland ecosystems. However, the relative importance of different facets of biodiversity underlying the diversity-stability relationship remains unclear. Here we use data from 39 grassland biodiversity experiments and structural equation modelling to investigate the roles of species richness, phylogenetic diversity and both the diversity and community-weighted mean of functional traits representing the 'fast-slow' leaf economics spectrum in driving the diversity-stability relationship. We found that high species richness and phylogenetic diversity stabilize biomass production via enhanced asynchrony in the performance of co-occurring species. Contrary to expectations, low phylogenetic diversity enhances ecosystem stability directly, albeit weakly. While the diversity of fast-slow functional traits has a weak effect on ecosystem stability, communities dominated by slow species enhance ecosystem stability by increasing mean biomass production relative to the standard deviation of biomass over time. Our in-depth, integrative assessment of factors influencing the diversity-stability relationship demonstrates a more multicausal relationship than has been previously acknowledged.
Soils harbour some of the most diverse microbiomes on Earth
and are essential for both nutrient cycling and carbon storage.
To understand soil functioning, it is necessary to model the
global distribution patterns and functional gene repertoires of
soil microorganisms, as well as the biotic and environmental
associations between the diversity and structure of both bacterial
and fungal soil communities1–4. Here we show, by leveraging
metagenomics and metabarcoding of global topsoil samples (189
sites, 7,560 subsamples), that bacterial, but not fungal, genetic
diversity is highest in temperate habitats and that microbial gene
composition varies more strongly with environmental variables than
with geographic distance. We demonstrate that fungi and bacteria
show global niche differentiation that is associated with contrasting
diversity responses to precipitation and soil pH. Furthermore, we
provide evidence for strong bacterial–fungal antagonism, inferred
from antibiotic-resistance genes, in topsoil and ocean habitats,
indicating the substantial role of biotic interactions in shaping
microbial communities. Our results suggest that both competition
and environmental filtering affect the abundance, composition
and encoded gene functions of bacterial and fungal communities,
indicating that the relative contributions of these microorganisms
to global nutrient cycling varies spatially.
Explaining the large-scale diversity of soil organisms that drive biogeochemical processes-and their responses to environmental change-is critical. However, identifying consistent drivers of belowground diversity and abundance for some soil organisms at large spatial scales remains problematic. Here we investigate a major guild, the ectomycorrhizal fungi, across European forests at a spatial scale and resolution that is-to our knowledge-unprecedented, to explore key biotic and abiotic predictors of ectomycorrhizal diversity and to identify dominant responses and thresholds for change across complex environmental gradients. We show the effect of 38 host, environment, climate and geographical variables on ectomycorrhizal diversity, and define thresholds of community change for key variables. We quantify host specificity and reveal plasticity in functional traits involved in soil foraging across gradients. We conclude that environmental and host factors explain most of the variation in ectomycorrhizal diversity, that the environmental thresholds used as major ecosystem assessment tools need adjustment and that the importance of belowground specificity and plasticity has previously been underappreciated.
Findings of immense microbial diversity are at odds with observed functional redundancy, as competitive exclusion should hinder coexistence. Tradeoffs between dispersal and competitive ability could resolve this contradiction, but the extent to which they influence microbial community assembly is unclear. Because fungi influence the biogeochemical cycles upon which life on earth depends, understanding the mechanisms that maintain the richness of their communities is critically important. Here, we focus on ectomycorrhizal fungi, which are microbial plant mutualists that significantly affect global carbon dynamics and the ecology of host plants. Synthesizing theory with a decade of empirical research at our study site, we show that competition-colonization tradeoffs structure diversity in situ and that models calibrated only with empirically derived competition-colonization tradeoffs can accurately predict species-area relationships in this group of key eukaryotic microbes. These findings provide evidence that competition-colonization tradeoffs can sustain the landscape-scale diversity of microbes that compete for a single limiting resource.
A global map of soil bacteria
Soil bacteria play key roles in regulating terrestrial carbon dynamics, nutrient cycles, and plant productivity. However, the natural histories and distributions of these organisms remain largely undocumented. Delgado-Baquerizo et al. provide a survey of the dominant bacterial taxa found around the world. In soil collections from six continents, they found that only 2% of bacterial taxa account for nearly half of the soil bacterial communities across the globe. These dominant taxa could be clustered into ecological groups of co-occurring bacteria that share habitat preferences. The findings will allow for a more predictive understanding of soil bacterial diversity and distribution.
Science , this issue p. 320
Tree planting and natural regeneration contribute to the ongoing effort to restore Earth's forests. Our review addresses how the plant microbiome can enhance the survival of planted and naturally regenerating seedlings and serve in long-term forest carbon capture and the conservation of biodiversity. We focus on fungal leaf endophytes, ubiquitous defensive symbionts that protect against pathogens. We first show that fungal and oomycetous pathogen richness varies greatly for tree species native to the United States ( n = 0–876 known pathogens per US tree species), with nearly half of tree species either without pathogens in these major groups or with unknown pathogens. Endophytes are insurance against the poorly known and changing threat of tree pathogens. Next, we reviewed studies of plant-phyllosphere feedback, but knowledge gaps prevented us from evaluating whether adding conspecific leaf litter to planted seedlings promotes defensive symbiosis, analogous to adding soil to promote positive feedback. Finally, we discuss research priorities for integrating the plant microbiome into efforts to expand Earth's forests.
Expected final online publication date for the Annual Review of Phytopathology, Volume 60 is August 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Global agriculture is dominated by a handful of species that currently supply a huge proportion of our food and feed. It additionally faces the massive challenge of providing food for 10 billion by 2050 despite increasing environmental deterioration. One way to better plan production in the face of current and continuing climate change is to better understand how our domestication of these crops included their adaptation to environments that were highly distinct from those of their centre of origin. There are many prominent examples of this including the development of temperate maize and the alteration of daylength requirements in potato. Despite the pre‐eminence of some 15 crops, more than 50,000 species are edible, with 7,000 of these considered semi‐cultivated. Opportunities afforded by next generation sequencing technologies alongside other methods including metabolomics and high‐throughput phenotyping are starting to contribute to a better characterization of a handful of these species. Moreover, the first examples of de novo domestication have appeared, whereby key target genes are modified in a wild species in order to confer predictable traits of agronomic value. Here we review the scale of the challenge, drawing extensively on the characterization of past agriculture to suggest informed strategies on which the breeding of future climate resilient crops can be based.
The plant microbiome is critical to plant health and is degraded with anthropogenic disturbance. However, the value of re‐establishing the native microbiome is rarely considered in ecological restoration. Arbuscular mycorrhizal (AM) fungi are particularly important microbiome components, as they associate with most plants, and later successional grassland plants are strongly responsive to native AM fungi. With five separate sites across the United States, we inoculated mid‐ and late successional plant seedlings with one of three types of native microbiome amendments: 1) whole rhizosphere soil collected from local old‐growth, undisturbed grassland communities in Illinois, Kansas, or Oklahoma, 2) laboratory cultured AM fungi from these same old‐growth grassland sites or 3) no microbiome amendment. We also seeded each restoration with a diverse native seed mixture. Plant establishment and growth was followed for three growing seasons. The reintroduction of soil microbiome from native ecosystems improved restoration establishment. Including only native arbuscular mycorrhizal fungal communities produced similar improvements in plant establishment as what was found with whole soil microbiome amendment. These findings were robust across plant functional groups. Inoculated plants (amended with either AM fungi or whole soil) also grew more leaves and were generally taller during the three growing seasons. Synthesis and Applications Our research shows that mycorrhizal fungi can accelerate plant succession and that the reintroduction of both whole soil and laboratory cultivated native mycorrhizal fungi can be used as tools to improve native plant restoration following anthropogenic disturbance.
Arbuscular mycorrhizal fungi (AMF) are plant symbionts that promote plant growth and provide important plant and ecosystem functions. These abilities have great economical potential which has resulted in an increasing number of commercially available AMF inoculants. Here, we present the results of a global study in which we evaluate the effectiveness of 28 commercial AMF inoculants to colonize host plants under greenhouse and field conditions. This evaluation includes three independent studies across three continents (Australia, Europe, and North America). The Australian and European studies tested 25 different commercial AMF inoculants in non-sterilized and sterilized soils under greenhouse conditions and compared them against laboratory cultures of the AMF Rhizophagus irregularis. This is supplemented by the North American study which evaluated the effects of three commercial inoculants under field conditions. In the greenhouse trials using non-sterilized soil, we observed that the addition of commercial inoculants did not lead to enhanced mycorrhizal colonization and inoculation increased plant biomass in only one out of 25 treatments. In sterilized soil, 84% of the mycorrhizal inoculants did not lead to mycorrhizal root colonization, demonstrating that these products did not contain viable propagules. In contrast, the laboratory cultures of the AM fungus Rhizophagus irregularis resulted in substantial root colonization (48% and 79%) in the Australian and European bioassay. Moreover, only five out of 25 treatments enhanced plant biomass when added to sterilized soil. Metagenomic analysis of field roots in the North American field trial revealed changes in the mycorrhizal community after inoculation. For one inoculant, this was accompanied by increased biomass production. This global evaluation of commercial inoculants raises concerns over unreliable products which do not contain viable propagules and do not result in mycorrhizal root colonization. Under field conditions, effects on plant growth are dependent on changes within the mycorrhizal community. The results of this study highlight the need for standardized quality control of AMF inoculants and further research on their establishment and effects under field conditions.
Beneficial microbes such as plant mutualistic fungi, hold the promise of ameliorating challenges faced in native plant conservation such as disease management. As an alternative to costly chemical pest control, conservation efforts could potentially harness the benefits of plant mutualistic fungi to aid in defense and disease resistance, but there are few tests of this notion. We set out to test the efficacy of controlling a common foliar pathogen, the powdery mildew Neoerysiphe galeopsidis, by inoculating the endangered Hawaiian plant species Phyllostegia kaalaensis with potentially beneficial members of its wild-type mycobiome. We tested whether inoculating plants with above or belowground fungal mutualists, or both, led to increased disease resistance in the host. We found that while all treatments reduced average disease incidence, colonization by the foliar yeast Moesziomyces aphidis was the only treatment to do so significantly. These results provide an exciting new strategy for plant conservation practices.
Fire has always been a driving factor of life on Earth. Now that mankind has definitely joined the other environmental forces in shaping the planet, lots of species are threatened by human-induced variation in fire regimes. Soil-dwelling organisms, i.e., those organisms that primarily live in soil, suffer the numerous and different consequences of fire occurrence that are, however, often overlooked compared to those on vegetation and wildlife. Most of these organisms live in the uppermost soil layer, where fire-imposed temperatures on the ground are the highest insofar as they are lethal or dangerously upset natural habitats.
This contribution is a reasoned collation of findings from a number of works conducted worldwide that aims to gain insight into the immediate and longer-term impacts of single or repeated wild or prescribed fires on one group of soil-dwelling organisms or more.
In fire-prone ecosystems, fire is a controlling factor of soil biota biodiversity and activity, but also where it is infrequent its ecological footprint can be substantial and lasting. Generally, the immediate fire impact on soil biota is strictly related to the peak temperatures reached on the ground and their duration, and on a set of soil properties and water content. Vertebrates can escape overheating death by running away, searching for wet niches or burrowing deep into soil. Invertebrates and microorganisms, which have little or no mobility, succumb more easily to fire, but make up for this intrinsic vulnerability thanks to their greater fecundity at the population level.
Fire or burn severity, which can generally be defined as loss of organic matter aboveground and belowground, is the key factor of the indirect fire effects on soil-dwelling biota; whereas controlled burns do not often imply any substantial and lasting shift from the original situation, extreme and vast wildfires can have major consequences that may be severer than direct killing. In fact lairs are devastated, nutrient pools are heavily affected, food webs are upset, soil temperature and moisture regimes change, and toxic pyrogenic compounds remain in soil. All types of organisms can recolonise the burned area from their sanctuaries, provided that land use does not change, e.g., to pastures or arable fields, and prompt enough vegetation re-sprouting and/or encroachment prevent substantial soil erosion. Each major taxon has genera or species with useful traits and behaviours to resist fire or to recover from its unwelcome environmental legacy sooner than others. If burned soil does not undergo other fires that occur too closely together for the typical fire regime of that particular area, most of its living components are generally capable of returning to pre-fire levels in times that depend on a series of factors, such as fire severity and post-fire rainfall.
High-throughput DNA sequencing has dramatically transformed several areas of biodiversity research including mycology. Despite limitations, high-throughput sequencing is nowadays a predominant method to characterize the alpha and beta diversity of fungal communities. Across the papers utilizing high-throughput sequencing approaches to study natural habitats in terrestrial ecosystems worldwide, > 200 studies published until 2019 have generated over 250 million sequences of the primary mycological metabarcoding marker, the nuclear ribosomal internal transcribed spacer 2 (ITS2). Here we show that at a 97% sequence similarity threshold, the total richness of non-singleton fungal taxa across the studies published so far is 1.08 million, mostly Ascomycota (56.8% of the taxa) and Basidiomycota (36.7% of the taxa). The Chao-1 estimate of the total extant fungal diversity based on this dataset is 6.28 million taxa, representing a conservative estimate of global fungal species richness. Soil and litter represent the habitats with the highest alpha diversity of fungi followed by air, plant shoots, plant roots and deadwood with Chao-1 predictions, for samples containing 5000 sequences, of 1219, 569, 392, 228, 215 and 140 molecular species, respectively. Based on the high-throughput sequencing data, the highest proportion of unknown fungal species is associated with samples of lichen and plant tissues. When considering the use of high-throughput sequencing for the estimation of global fungal diversity, the limitations of the method have to be taken into account, some of which are sequencing platform-specific while others are inherent to the metabarcoding approaches of species representation. In this respect, high-throughput sequencing data can complement fungal diversity predictions based on methods of traditional mycology and increase our understanding of fungal biodiversity.
A monitoring and indicator system can inform policy
Largely driven by the corporate sector, the recent surge of interest in trees as a solution to climate change has a distinct emphasis on planting trees. Realizing anticipated benefits will require managing the risks and trade-offs of land-use interventions and embracing the imperative of protecting existing forests.
Grasslands are among the most threatened terrestrial biomes, and habitat conservation alone will be insufficient to meet biodiversity goals. While restoration of indigenous grasslands is a priority, conflict with economic objectives means that incorporation of alternative habitats is necessary to offset grassland loss. With up to 800,000 km2 of land affected by mining globally, there is an opportunity to create additional grassland habitat in post‐mining landscapes. We aimed to assess whether co‐introduction of native arbuscular mycorrhizal (AM) fungi and plants is an efficient means of initializing species rich vegetation recovery in barren post‐mining landscapes. We established an experiment in three post‐mining areas in Estonia, where we seeded plots with native plant seeds and inoculated them with trap cultured native AM fungi from a similar habitat. We measured the abundance and composition of soil AM fungal and aboveground plant communities in two consecutive years using relevés, high‐throughput sequencing and fatty acid profiling. Our results demonstrate that co‐introduction of native plants and AM fungi is an effective way to establish species rich vegetation in post‐mining areas. Co‐introduction of symbiotic partners resulted in higher richness, diversity and abundance of plants and AM fungi than when either partner was introduced individually. However, the plant and AM fungal communities in sown and inoculated plots were not distinct from those in uninoculated treatments; they rather formed a subset of all taxa present on the sites but exhibited higher diversity than uninoculated plots. Synthesis and applications: This study shows that managing the below‐ground microbiome is an essential part of vegetation restoration. The availability of symbiotic partners can be considered a key aspect determining the diversity of restored vegetation. Targeted inoculations with native and habitat‐specific AM fungi could therefore increase restoration success.
Many factors influence global change
Global environmental change is driven by multiple natural and anthropogenic factors. With a focus on global change as it affects soils, Rillig et al. point out that nearly all published studies consider just one or two factors at a time (see the Perspective by Manning). In a laboratory experiment, they tested 10 drivers of global change both individually and in combination, at levels ranging from 2 to 10 factors. They found that soil properties, processes, and microbial communities could not be predicted from single-effect responses and that multiple factors in combination produced unsuspected responses. They concluded that single-factor studies remain important for uncovering mechanisms but that global change biology needs to embrace more fully the multitude of drivers impinging on ecosystems.
Science , this issue p. 886 ; see also p. 801
Microorganisms drive several processes needed for robust plant growth and
health.Harnessing microbial functions is thus key to productive and sustainable
food production.Molecular methods have led to a greater understanding
of the soil microbiome composition. However, translating species or
gene composition into microbiome functionality remains a challenge. Community
ecology concepts such as the biodiversity–ecosystem functioning
framework may help predict the assembly and function of plant-associated
soil microbiomes.Higher diversity can increase the number and resilience of
plant-beneficial functions that can be coexpressed and unlock the expression
of plant-beneficial traits that are hard to obtain from any species in isolation.
We combine well-established community ecology concepts with molecular
microbiology into a workable framework that may enable us to predict and
enhance soil microbiome functionality to promote robust plant growth in a
global change context.
Increasing evidence suggests that specific interactions between microbial decomposers and plant litter, named home field advantage (HFA), influence litter breakdown. However, we still have limited understanding of whether HFA relates to specific microbiota, and whether specialized microbes originate from the soil or from the leaf microbiome. Here, we disentangle the roles of soil origin, litter types, and the microbial community already present on the leaf litter in determining fungal community composition on decomposing leaf litter and HFA. We collected litters and associated soil samples from a secondary succession gradient ranging from herbaceous vegetation on recently abandoned ex‐arable fields to forest representing the end stage of succession. In a greenhouse, sterilized and unsterilized leaf litters were decomposed for 12 months in soils from early to late successional stages according to a full factorial design. At the end, we examined fungal community composition on the decomposing litter. Fungal communities on decomposed late‐successional litter in late‐successional soil differed from those in early‐ and mid‐successional stage litter and soil combinations. Soil source had the strongest impact on litter fungal composition when using sterilized litter, while the impact of litter type was strongest when using unsterilized litter. Overall, we observed HFA, as litter decomposition was accelerated in home soils. Increasing HFA did not relate to the dissimilarity in overall fungal composition, but there was increasing dissimilarity in the relative abundance of the most dominant fungal taxon between decomposing litter in home and away soils. We conclude that early, mid and late succession litter types did not exert strong selection effects on colonization by microorganisms from the soil species pool. Instead, fungal community composition on decomposing litter differed substantially between litter types for unsterilized litter, suggesting that the leaf microbiome, either directly or indirectly, is an important determinant of fungal community composition on decomposing leaves. HFA related most strongly to the abundance of the most dominant fungal taxa on the decomposing litter, suggesting that HFA may be attributed to some specific dominant fungi rather than to responses of the whole fungal community. This article is protected by copyright. All rights reserved.
Human activities are accelerating global biodiversity change and have resulted in severely threatened ecosystem services. A large proportion of terrestrial biodiversity is harbored by soil, but soil biodiversity has been neglected from many global biodiversity assessments and conservation actions, and our understanding of global patterns of soil biodiversity remains limited. In particular, the extent to which hotspots and coldspots of aboveground and soil biodiversity overlap is not clear. We examined global patterns of overlap by mapping indices of aboveground (mammals, birds, amphibians, vascular plants) and soil (bacteria, fungi, macrofauna) biodiversity. Our analysis indicated that areas of mismatch between aboveground and soil biodiversity covered 27% of the Earth's terrestrial surface. The temperate broadleaf and mixed forests biome had the highest proportion of grid cells with high aboveground biodiversity but low soil biodiversity, while the boreal and tundra biomes had higher soil biodiversity but low aboveground biodiversity. While more data on soil biodiversity is needed, both to cover geographic gaps and to include additional taxa, our results suggest that protecting aboveground biodiversity may not sufficiently reduce threats to soil biodiversity. Given the functional importance of soil biodiversity and the role of soils for human well‐being, soil biodiversity should be further considered in policy agendas and conservation actions by adapting management practices to sustain soil biodiversity and considering soil biodiversity when designing protected areas.
This article is protected by copyright. All rights reserved
Humans have dramatically increased atmospheric nitrogen (N) deposition globally. At the coarsest resolution, N deposition is correlated with shifts from ectomycorrhizal (EcM) to arbuscular mycorrhizal (AM) tree dominance. At finer resolution, ectomycorrhizal fungal (EcMF) and arbuscular mycorrhizal fungal (AMF) communities respond strongly to long-term N deposition with the disappearance of key taxa. Conifer-associated EcMF are more sensitive than other EcMF, with current estimates of critical loads at 5–6 kg ha⁻¹ yr⁻¹ for the former and 10–20 kg ha⁻¹ yr⁻¹ for the latter. Where loads are exceeded, strong plant-soil and microbe-soil feedbacks may slow recovery rates after abatement of N deposition. Critical loads for AMF and tropical EcMF require additional study. In general, the responses of EcMF to N deposition are better understood than those of AMF because of methodological tractability. Functional consequences of EcMF community change are linked to decreases by fungi with medium-distance exploration strategies, hydrophobic walls, proteolytic capacity, and perhaps peroxidases for acquiring N from soil organic matter. These functional losses may contribute to declines in forest floor decomposition under N deposition. For AMF, limited capacity to directly access complexed organic N may reduce functional consequences, but research is needed to test this hypothesis. Mycorrhizal biomass often declines with N deposition, but the relative contributions of alternate mechanisms for this decline (lower C supply, higher C cost, physiological stress by N) have not been quantified. Furthermore, fungal biomass and functional responses to N inputs probably depend on ecosystem P status, yet how N deposition-induced P limitation interacts with belowground C flux and mycorrhizal community structure and function is still unclear. Current ‘omic analyses indicate potential functional differences among fungal lineages and should be integrated with studies of physiology, host nutrition, growth and health, fungal and plant community structure, and ecosystem processes. Forest mycorrhizal fungal community composition responds strongly to N deposition across broad ranges of spatial, temporal and phylogenetic scales, with functional consequences—including altered tree nutrition and C, N, and P cycling—that are substantial but only partially understood.
Fungi are important members of soil microbial communities in row-crop and grassland soils, provide essential ecosystem services such as nutrient cycling, organic matter decomposition, and soil structure, but fungi are also more sensitive to physical disturbance than other microorganisms. Adoption of conservation management practices such as no-till and cover cropping shape the structure and function of soil fungal communities. No-till eliminates or greatly reduces the physical disturbance that re-distributes organisms and nutrients in the soil profile and disrupts fungal hyphal networks, while cover crops provide additional types and greater abundance of organic carbon sources. In a long-term, row crop field experiment in California's Central Valley we hypothesized that a more diverse and plant symbiont-enriched fungal soil community would develop in soil managed with reduced tillage practices and/or cover crops compared to standard tillage and no cover crops. We measured the interacting effects of tillage and cover cropping on fungal communities based on fungal ITS sequence assigned to ecological guilds. Functional groups within fungal communities were most sensitive to long-term tillage practices, with 45% of guild-assigned taxa responding to tillage, and a higher proportion of symbiotroph taxa under no-till. In contrast, diversity measures reflected greater sensitivity to cover crops, with higher phylogenetic diversity observed in soils managed with cover crops, though only 10% of guild-assigned taxa responded to cover crops. The relative abundance of pathotrophs did not vary across the management treatments. Cover cropping increased species diversity, while no-till shifted the symbiotroph:saprotroph ratio to favor symbiotrophs. These management-induced shifts in fungal community composition could lead to greater ecosystem resilience and provide greater access of crops to limiting resources.
Mycorrhizal inoculation can enhance outcomes of ecological restoration, but the benefits may be context-dependent. Here, we performed a meta-analysis of field studies to elucidate conditions in which adding mycorrhizal fungi enhances restoration success. We found inoculation increased plant biomass by an average effect size of 1.7 in 70 independent comparisons from 26 field-based studies, with the largest increases to N-fixing woody plants, C4-grasses and plants growing in soils with low plant-available P. Growth responses to inoculation increased with time for the first 3 yr after inoculation, especially for N-fixing woody plants and plants growing in severely altered soils. We found that mycorrhizal inoculation increased species richness of restored plant communities by 30%, promoted establishment of target species, and enhanced similarity of restored to reference communities. We conclude that the addition of mycorrhizal fungi to restoration sites can facilitate rapid establishment of vegetation cover, and restoration of diverse plant communities more akin to reference sites.