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Most of Earths trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earths land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grew Pinus muricata plants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.IMPORTANCEUnderstanding how soil microbes interact with one another and their host plant will help us combat the negative effects that climate change has on terrestrial ecosystems. Unfortunately, we lack a clear understanding of how the presence of ectomycorrhizal fungi (EcMF)-one of the most dominant soil microbial groups on Earth-shapes belowground organic resources and the composition of bacterial communities. To address this knowledge gap, we profiled lipid and non-lipid metabolites in soils and plant roots, characterized soil bacterial communities, and compared soils amended either with or without EcMF. Our results show that the presence of EcMF changes soil organic resource availability, impacts the proliferation of different bacterial communities (in terms of both type and potential function), and primes plant root chemistry for pathogen suppression and energy conservation. Our findings therefore provide much-needed insight into how two of the most dominant soil microbial groups interact with one another and with their host plant.

Functional traits influence the assembly of microbial communities, but identifying these traits in the environment has remained challenging. We studied ectomycorrhizal fungal (EMF) communities inhabiting Populus trichocarpa roots distributed across a precipitation gradient in the Pacific Northwest, USA. We profiled these communities using taxonomic (meta-barcoding) and functional (metagenomic) approaches. We hypothesized that genes involved in fungal drought-stress tolerance and fungal mediated plant water uptake would be most abundant in drier soils. We were unable to detect support for this hypothesis; instead, the abundance of genes involved in melanin synthesis, hydrophobins, aquaporins, trehalose-synthases, and other gene families exhibited no significant shifts across the gradient. Finally, we studied variation in sequence homology for certain genes, finding that fungal communities in dry soils are composed of distinct aquaporin and hydrophobin gene sequences. Altogether, our results suggest that while EMF communities exhibit significant compositional shifts across this gradient, coupled functional turnover, at least as inferred using community metagenomics is limited. Accordingly, the consequences of these distinct EMF communities on plant water uptake remain critically unknown, and future studies targeting the expression of genes involved in drought stress tolerance are required.

The evolutionary and environmental factors that shape fungal biogeography are incompletely understood. Here, we assemble a large dataset consisting of previously generated mycobiome data linked to specific geographical locations across the world. We use this dataset to describe the distribution of fungal taxa and to look for correlations with different environmental factors such as climate, soil and vegetation variables. Our meta-study identifies climate as an important driver of different aspects of fungal biogeography, including the global distribution of common fungi as well as the composition and diversity of fungal communities. In our analysis, fungal diversity is concentrated at high latitudes, in contrast with the opposite pattern previously shown for plants and other organisms. Mycorrhizal fungi appear to have narrower climatic tolerances than pathogenic fungi. We speculate that climate change could affect ecosystem functioning because of the narrow climatic tolerances of key fungal taxa.

The breadth and depth of plant leaf metabolomes have been implicated in key interactions with plant enemies aboveground. In particular, divergence in plant species chemical composition—amongst neighbors, relatives, or both—is often suggested as a means of escape from insect herbivore enemies. Plants also experience strong pressure from enemies such as belowground pathogens; however, little work has been carried out to examine the evolutionary trajectories of species' specialized chemistries in both roots and leaves. Here, we examine the GCMS detectable phytochemistry (for simplicity, hereafter referred to as specialized volatile metabolites) of the tropical tree genus Protium, testing the hypothesis that phenotypic divergence will be weaker belowground compared to aboveground due to more limited dispersal by enemies. We found that, after controlling for differences in chemical richness, roots expressed less structurally diverse compounds than leaves, despite having higher numbers of specialized volatile metabolites, and that species' phylogenetic distance was only positively correlated with compound structural distance in roots, not leaves. Taken together, our results suggest that root specialized volatile metabolites exhibit significantly less phenotypic divergence than leaf specialized metabolites and may be under relaxed selection pressure from enemies belowground. [ABSTRACT FROM AUTHOR]

Specific interactions between bacteria and ectomycorrhizal fungi (EcMF) can benefit plant health, and saprotrophic soil fungi represent a potentially antagonistic guild to these mutualisms. Yet there is little field‐derived experimental evidence showing how the relationship among these three organismal groups manifests across time. To bridge this knowledge gap, we experimentally reduced EcMF in forest soils and monitored both bacterial and fungal soil communities over the course of a year. Our analyses demonstrate that soil trenching shifts the community composition of fungal communities towards a greater abundance of taxa with saprotrophic traits, and this shift is linked to a decrease in both EcMF and a common ectomycorrhizal helper bacterial genus, Burkholderia, in a time‐dependent manner. These results not only reveal the temporal nature of a widespread tripartite symbiosis between bacteria, EcMF and a shared host tree, but they also refine our understanding of the commonly referenced 'Gadgil effect' by illustrating the cascading effects of EcMF suppression and implicating soil saprotrophic fungi as potential antagonists on bacterial‐EcMF interactions. [ABSTRACT FROM AUTHOR]

Recent advancements in sequencing technology allowed researchers to better address the patterns and mechanisms involved in microbial environmental adaptation at large spatial scales. Here we investigated the genomic basis of adaptation to climate at the continental scale in Suillus brevipes, an ectomycorrhizal fungus symbiotically associated with the roots of pine trees. We used genomic data from 55 individuals in seven locations across North America to perform genome scans to detect signatures of positive selection and assess whether temperature and precipitation were associated with genetic differentiation. We found that S. brevipes exhibited overall strong population differentiation, with potential admixture in Canadian populations. This species also displayed genomic signatures of positive selection as well as genomic sites significantly associated with distinct climatic regimes and abiotic environmental parameters. These genomic regions included genes involved in transmembrane transport of substances and helicase activity potentially involved in cold stress response. Our study sheds light on large-scale environmental adaptation in fungi by identifying putative adaptive genes and providing a framework to further investigate the genetic basis of fungal adaptation.

The supply of nitrogen (N) constrains primary productivity in many ecosystems, raising the question "what controls the availability and cycling of N"? As a step toward answering this question, we evaluated N cycling processes and aspects of their regulation on a climate gradient on Kohala Volcano, Hawaii, USA. The gradient extends from sites receiving 3,000 mm/yr, and the pedology and dynamics of rock-derived nutrients in soils on the gradient are well understood. In particular, there is a soil process domain at intermediate rainfall within which ongoing weathering and biological uplift have enriched total and available pools of rock-derived nutrients substantially; sites at higher rainfall than this domain are acid and infertile as a consequence of depletion of rock-derived nutrients, while sites at lower rainfall are unproductive and subject to wind erosion. We found elevated rates of potential net N mineralization in the domain where rock-derived nutrients are enriched. Higher-rainfall sites have low rates of potential net N mineralization and high rates of microbial N immobilization, despite relatively high rates of gross N mineralization. Lower-rainfall sites have moderately low potential net N mineralization, relatively low rates of gross N mineralization, and rates of microbial N immobilization sufficient to sequester almost all the mineral N produced. Bulk soil δ15 N also varied along the gradient, from +4‰ at high rainfall sites to +14‰ at low rainfall sites, indicating differences in the sources and dynamics of soil N. Our analysis shows that there is a strong association between N cycling and soil process domains that are defined using soil characteristics independent of N along this gradient, and that short-term controls of N cycling can be understood in terms of the supply of and demand for N.

The supply of nitrogen (N) constrains primary productivity in many ecosystems, raising the question "what controls the availability and cycling of N"? As a step toward answering this question, we evaluated N cycling processes and aspects of their regulation on a climate gradient on Kohala Volcano, Hawaii, USA. The gradient extends from sites receiving 3,000 mm/yr, and the pedology and dynamics of rock-derived nutrients in soils on the gradient are well understood. In particular, there is a soil process domain at intermediate rainfall within which ongoing weathering and biological uplift have enriched total and available pools of rock-derived nutrients substantially; sites at higher rainfall than this domain are acid and infertile as a consequence of depletion of rock-derived nutrients, while sites at lower rainfall are unproductive and subject to wind erosion. We found elevated rates of potential net N mineralization in the domain where rock-derived nutrients are enriched. Higher-rainfall sites have low rates of potential net N mineralization and high rates of microbial N immobilization, despite relatively high rates of gross N mineralization. Lower-rainfall sites have moderately low potential net N mineralization, relatively low rates of gross N mineralization, and rates of microbial N immobilization sufficient to sequester almost all the mineral N produced. Bulk soil δ15 N also varied along the gradient, from +4‰ at high rainfall sites to +14‰ at low rainfall sites, indicating differences in the sources and dynamics of soil N. Our analysis shows that there is a strong association between N cycling and soil process domains that are defined using soil characteristics independent of N along this gradient, and that short-term controls of N cycling can be understood in terms of the supply of and demand for N.

Background. The extent to which ectomycorrhizal fungi mediate primary production, carbon storage, and nutrient remineralization in terrestrial ecosystems depends upon fungal community composition. However, the factors that govern community composition at the root system scale are not well understood. Here, we explore a potential tradeoff between ectomycorrhizal fungal competitive ability and enzymatic function. Methods. We grew Pinus muricata (Bishop Pine) seedlings in association with ectomycorrhizal fungi from three different genera in a fully factorial experimental design. We measured seedling growth responses, ectomycorrhizal abundance, and the root tip activity of five different extracellular enzymes involved in the mobilization of carbon and phosphorus. Results. We found an inverse relationship between competitiveness, quantified based on relative colonization levels, and enzymatic activity. Specifically, Thelephora terrestris, the dominant fungus, had the lowest enzyme activity levels, while Suillus pungens, the least dominant fungus, had the highest. Discussion. Our results identify a tradeoff between competition and function in ectomycorrhizal fungi, perhaps mediated by the competing energetic demands associated with competitive interactions and enzymatic production. These data suggest that mechanisms such as active partner maintenance by host trees may be important to maintaining "high-quality" ectomycorrhizal fungal partners in natural systems.

Ecologists have long acknowledged the importance of seed banks; yet, despite the fact that many plants rely on mycorrhizal fungi for survival and growth, the structure of ectomycorrhizal (ECM) fungal spore banks remains poorly understood. The primary goal of this study was to assess the geographic structure in pine-associated ECM fungal spore banks across the North American continent. Soils were collected from 19 plots in forests across North America. Fresh soils were pyrosequenced for fungal internal transcribed spacer (ITS) amplicons. Adjacent soil cores were dried and bioassayed with pine seedlings, and colonized roots were pyrosequenced to detect resistant propagules of ECM fungi. The results showed that ECM spore banks correlated strongly with biogeographic location, but not with the identity of congeneric plant hosts. Minimal community overlap was found between resident ECM fungi vs those in spore banks, and spore bank assemblages were relatively simple and dominated by Rhizopogon, Wilcoxina, Cenococcum, Thelephora, Tuber, Laccaria and Suillus. Similar to plant seed banks, ECM fungal spore banks are, in general, depauperate, and represent a small and rare subset of the mature forest soil fungal community. Yet, they may be extremely important in fungal colonization after large-scale disturbances such as clear cuts and forest fires.

Identifying the ecological processes that structure communities and the consequences for ecosystem function is a central goal of ecology. The recognition that fungi, bacteria, and viruses control key ecosystem functions has made microbial communities a major focus of this field. Because many ecological processes are apparent only at particular spatial or temporal scales, a complete understanding of the linkages between microbial community, environment, and function requires analysis across a wide range of scales. Here, we map the biological and functional geography of soil fungi from local to continental scales and show that the principal ecological processes controlling community structure and function operate at different scales. Similar to plants or animals, most soil fungi are endemic to particular bioregions, suggesting that factors operating at large spatial scales, like dispersal limitation or climate, are the first-order determinants of fungal community structure in nature. By contrast, soil extracellular enzyme activity is highly convergent across bioregions and widely differing fungal communities. Instead, soil enzyme activity is correlated with local soil environment and distribution of fungal traits within the community. The lack of structure-function relationships for soil fungal communities at continental scales indicates a high degree of functional redundancy among fungal communities in global biogeochemical cycles.

Climate change will likely shift plant and microbial distributions, creating geographic mismatches between plant hosts and essential microbial symbionts (e.g., ectomycorrhizal fungi, EMF). The loss of historical interactions, or the gain of novel associations, can have important consequences for biodiversity, ecosystem processes, and plant migration potential, yet few analyses exist that measure where mycorrhizal symbioses could be lost or gained across landscapes. Here, we examine climate change impacts on tree-EMF codistributions at the continent scale. We built species distribution models for 400 EMF species and 50 tree species, integrating fungal sequencing data from North American forest ecosystems with tree species occurrence records and long-term forest inventory data. Our results show the following: 1) tree and EMF climate suitability to shift toward higher latitudes; 2) climate shifts increase the size of shared tree-EMF habitat overall, but 35% of tree-EMF pairs are at risk of declining habitat overlap; 3) climate mismatches between trees and EMF are projected to be greater at northern vs. southern boundaries; and 4) tree migration lag is correlated with lower richness of climatically suitable EMF partners. This work represents a concentrated effort to quantify the spatial extent and location of tree-EMF climate envelope mismatches. Our findings also support a biotic mechanism partially explaining the failure of northward tree species migrations with climate change: reduced diversity of co-occurring and climate-compatible EMF symbionts at higher latitudes. We highlight the conservation implications for identifying areas where tree and EMF responses to climate change may be highly divergent. [ABSTRACT FROM AUTHOR]

Understanding how abiotic conditions mediate the outcome of biotic interactions is a key question in community ecology. This is particularly interesting in the case of mutualisms because changing environmental conditions may be a source of evolutionary or ecological instability in the relationship between symbiotic partners. For the mycorrhizal symbiosis, elevated nutrient levels may make the carbon cost to plants of supporting mycorrhizal fungi outweigh the benefits of mycorrhizal nutrient acquisition. In this study, we simulated the effects of post-fire nutrient enrichment on the ectomycorrhizal symbiosis between Rhizopogon occidentalis and Pinus muricata by using factorial combinations of soil heating, ash addition and mycorrhizal colonization. In general, the presence of R. occidentalis and the heat and ash treatments increased growth of P. muricata seedlings. However, significant interactions between the treatments indicated that there were context-dependent effects on seedling growth. Soil heating increased soil mineral nitrogen content, but did not decrease the benefit of mycorrhizal colonization relative to unheated controls. This appeared to be driven by a decrease in the proportion of the root system occupied by R. occidentalis, indicating that host-plants can optimize colonization in a way that maximizes growth. Because seedlings in heat-treated soils were larger than unheated controls, reduced percent colonization did not cause any decrease in fungal biomass in heat-treated soils. Since there was no decrease in the performance of either partner, our results show that, in this system, ectomycorrhizal mutualisms are likely robust within the natural degree of environmental variability caused by moderate intensity wildfires.