Ectomycorrhizal fungi alter soil food webs and the functional potential of bacterial communities.

Most of Earth's trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earth's 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.

Fungal Fight Club: phylogeny and growth rate predict competitive outcomes among ectomycorrhizal fungi.

Ectomycorrhizal fungi are among the most prevalent fungal partners of plants and can constitute up to one-third of forest microbial biomass. As mutualistic partners that supply nutrients, water, and pathogen defense, these fungi impact host plant health and biogeochemical cycling. Ectomycorrhizal fungi are also extremely diverse, and the community of fungal partners on a single plant host can consist of dozens of individuals. However, the factors that govern competition and coexistence within these communities are still poorly understood. In this study, we used in vitro competitive assays between five ectomycorrhizal fungal strains to examine how competition and pH affect fungal growth. We also tested the ability of evolutionary history to predict the outcomes of fungal competition. We found that the effects of pH and competition on fungal performance varied extensively, with changes in growth media pH sometimes reversing competitive outcomes. Furthermore, when comparing the use of phylogenetic distance and growth rate in predicting competitive outcomes, we found that both methods worked equally well. Our study further highlights the complexity of ectomycorrhizal fungal competition and the importance of considering phylogenetic distance, ecologically relevant traits, and environmental conditions in predicting the outcomes of these interactions.

Modified source-sink dynamics govern resource exchange in ectomycorrhizal symbiosis.

Ectomycorrhizal symbiosis between roots and fungi is founded on the movement of carbon from plants to fungi, and of soil resources from fungi to plants. Framing this movement as a trade can facilitate an understanding of how this mutualism has developed over evolutionary time, but fails to explain experimental observations of carbon and nutrient movement. Here, I propose that source-sink dynamics are an essential basic model to explain the movement of plant and fungal resources, which may be modified by plant immune response, variability in fungal molecular repertoires, and competition in the soil. Source-sink dynamics provide testable hypotheses to illuminate mechanisms of ectomycorrhizal resource movement and its consequences for mutualism stability and forest function under climate change.

Does resource exchange in ectomycorrhizal symbiosis vary with competitive context and nitrogen addition?

Ectomycorrhizal symbiosis is essential for the nutrition of most temperate forest trees and helps regulate the movement of carbon (C) and nitrogen (N) through forested ecosystems. The factors governing the exchange of plant C for fungal N, however, remain obscure. Because competition and soil resources may influence ectomycorrhizal resource movement, we performed a 10-month split-root microcosm study using Pinus muricata seedlings with Thelephora terrestris, Suillus pungens, or no ectomycorrhizal fungus, under two N concentrations in artificial soil. Fungi competed directly with roots and indirectly with each other. We used stable isotope enrichment to track plant photosynthate and fungal N. For T. terrestris, plants received N commensurate with the C given to their fungal partners. Thelephora terrestris was a superior mutualist under high-N conditions. For S. pungens, plant C and fungal N exchange were not coupled. However, in low-N conditions, plants preferentially allocated C to S. pungens rather than T. terrestris. Our results suggest that ectomycorrhizal resource transfer depends on competitive and nutritional context. Plants can exchange C for fungal N, but coupling of these resources can depend on the fungal species and soil N. Understanding the diversity of fungal strategies, and how they change with environmental context, reveals mechanisms driving this important symbiosis.

New wrinkles in an old paradigm: neighborhood effects can modify the structure and specificity of Alnus-associated ectomycorrhizal fungal communities.

Host identity has been recognized as a key determinant of the structure of ectomycorrhizal (ECM) fungal communities, but the importance of neighboring ECM hosts is less well understood. To investigate the relative importance of host and neighborhood effects, we examined the ECM fungal communities associated with Alnus rhombifolia, a host of specific ECM fungi, and Betula occidentalis, a host of generalist ECM fungi. We hypothesized that the host-specific Alnus-associated ECM fungal community would not be susceptible to the influence of plant neighborhood, while the generalist Betula-associated community would. ECM fungal communities on both hosts were characterized using ITS sequences derived from conspecific and heterospecific host settings at a field site in western Idaho, USA, and from a growth chamber bioassay. In the field study, the Betula neighborhood added minor constituents to the Alnus ECM fungal community, while in the bioassay, late planting of Betula generated strong priority effects that allowed the established Alnus neighborhood to control the structure of the Betula community. Our results indicate that while host identity acts as a primary filter on the composition and diversity of ECM fungal communities, proximity to a closely related host can mediate significant changes in community structure.