The extent to which ectomycorrhizal (ECM) fungi decay soil organic matter (SOM) has implications for accurately predicting forest ecosystem response to climate change. Investigating the distribution of gene traits associated with SOM decay among ectomycorrhizal fungal communities could improve understanding of SOM dynamics and plant nutrition. We hypothesized that soil inorganic nitrogen (N) availability structures the distribution of ECM fungal genes associated with SOM decay and, specifically, that ECM fungal communities occurring in inorganic N‐poor soils have greater SOM decay potential. To test this hypothesis, we paired amplicon and shotgun metagenomic sequencing of 60 ECM fungal communities associating with Ectomycorrhizal fungal communities occurring in low inorganic N soils were enriched in gene families involved in the decay of lignin, cellulose, and chitin. Ectomycorrhizal fungal community composition was the strongest driver of shifts in metagenomic estimates of fungal decay potential. Our study simultaneously illuminates the identity of key ECM fungal taxa and gene families potentially involved in the decay of SOM, and we link rhizomorphic and medium‐distance hyphal morphologies with enhanced SOM decay potential. Coupled shifts in ECM fungal community composition and community‐level decay gene frequencies are consistent with outcomes of trait‐mediated community assembly processes.
Interactions between soil nitrogen (N) availability, fungal community composition, and soil organic matter (SOM) regulate soil carbon (C) dynamics in many forest ecosystems, but context dependency in these relationships has precluded general predictive theory. We found that ectomycorrhizal (ECM) fungi with peroxidases decreased with increasing inorganic N availability across a natural inorganic N gradient in northern temperate forests, whereas ligninolytic fungal saprotrophs exhibited no response. Lignin‐derived SOM and soil C were negatively correlated with ECM fungi with peroxidases and were positively correlated with inorganic N availability, suggesting decay of lignin‐derived SOM by these ECM fungi reduced soil C storage. The correlations we observed link SOM decay in temperate forests to tradeoffs in tree N nutrition and ECM composition, and we propose SOM varies along a single continuum across temperate and boreal ecosystems depending upon how tree allocation to functionally distinct ECM taxa and environmental stress covary with soil N availability.
more » « less- PAR ID:
- 10445802
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 25
- Issue:
- 2
- ISSN:
- 1461-023X
- Format(s):
- Medium: X Size: p. 391-404
- Size(s):
- p. 391-404
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Summary Quercus rubra along a natural soil inorganic N gradient. -
Druzhinina, Irina S. (Ed.)ABSTRACT Trees associating with different mycorrhizas often differ in their effects on litter decomposition, nutrient cycling, soil organic matter (SOM) dynamics, and plant-soil interactions. For example, due to differences between arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) tree leaf and root traits, ECM-associated soil has lower rates of C and N cycling and lower N availability than AM-associated soil. These observations suggest that many groups of nonmycorrhizal fungi should be affected by the mycorrhizal associations of dominant trees through controls on nutrient availability. To test this overarching hypothesis, we explored the influence of predominant forest mycorrhizal type and mineral N availability on soil fungal communities using next-generation amplicon sequencing. Soils from four temperate hardwood forests in southern Indiana, United States, were studied; three forests formed a natural gradient of mycorrhizal dominance (100% AM tree basal area to 100% ECM basal area), while the fourth forest contained a factorial experiment testing long-term N addition in both dominant mycorrhizal types. We found that overall fungal diversity, as well as the diversity and relative abundance of plant pathogenic and saprotrophic fungi, increased with greater AM tree dominance. Additionally, tree community mycorrhizal associations explained more variation in fungal community composition than abiotic variables, including soil depth, SOM content, nitrification rate, and mineral N availability. Our findings suggest that tree mycorrhizal associations may be good predictors of the diversity, composition, and functional potential of soil fungal communities in temperate hardwood forests. These observations help explain differing biogeochemistry and community dynamics found in forest stands dominated by differing mycorrhizal types. IMPORTANCE Our work explores how differing mycorrhizal associations of temperate hardwood trees (i.e., arbuscular [AM] versus ectomycorrhizal [ECM] associations) affect soil fungal communities by altering the diversity and relative abundance of saprotrophic and plant-pathogenic fungi along natural gradients of mycorrhizal dominance. Because temperate hardwood forests are predicted to become more AM dominant with climate change, studies examining soil communities along mycorrhizal gradients are necessary to understand how these global changes may alter future soil fungal communities and their functional potential. Ours, along with other recent studies, identify possible global trends in the frequency of specific fungal functional groups responsible for nutrient cycling and plant-soil interactions as they relate to mycorrhizal associations.more » « less
-
more » « less
Abstract Plant–mycorrhizal interactions mediate plant nitrogen (N) limitation and can inform model projections of the duration and strength of the effect of increasing CO2on plant growth. We present dendrochronological evidence of a positive, but context-dependent fertilization response of
Quercus rubra L . to increasing ambient CO2(iCO2) along a natural soil nutrient gradient in a mature temperate forest. We investigated this heterogeneous response by linking metagenomic measurements of ectomycorrhizal (ECM) fungal N-foraging traits and dendrochronological models of plant uptake of inorganic N and N bound in soil organic matter (N-SOM). N-SOM putatively enhanced tree growth under conditions of low inorganic N availability, soil conditions where ECM fungal communities possessed greater genomic potential to decay SOM and obtain N-SOM. These trees were fertilized by 38 years of iCO2. In contrast, trees occupying inorganic N rich soils hosted ECM fungal communities with reduced SOM decay capacity and exhibited neutral growth responses to iCO2. This study elucidates how the distribution of N-foraging traits among ECM fungal communities govern tree access to N-SOM and subsequent growth responses to iCO2. -
Yavitt, Joseph B. (Ed.)As global change shifts the species composition of forests, we need to understand which species characteristics affect soil organic matter cycling to predict future soil carbon (C) storage. Recently, whether a tree species forms a symbiosis with arbuscular (AM) versus ectomycorrhizal (EcM) fungi has been suggested as a strong predictor of soil carbon storage, but there is wide variability within EcM systems. In this study, we investigated how mycorrhizal associations and the species composition of canopy trees and mycorrhizal fungi relate to the proportion of soil C and nitrogen (N) in mineral-associations and soil C:N across four sites representing distinct climates and tree communities in the Eastern U.S. broadleaf forest biome. In two of our sites, we found the expected relationship of declining mineral-associated C and N and increasing soil C:N ratios as the basal area of EcM-associating trees increased. However, across all sites these soil properties strongly correlated with canopy tree and fungal species composition. Sites where the expected pattern with EcM basal area was observed were 1) dominated by trees with lower quality litter in the Pinaceae and Fagaceae families and 2) dominated by EcM fungi with medium distance exploration type hyphae, melanized tissues, and the potential to produce peroxidases. This observational study demonstrates that differences in soil organic matter between AM andEcM systems are dependent on the taxa of trees and EcM fungi involved. Important information is lost when the rich mycorrhizal symbiosis is reduced to two categories.more » « less
-
more » « less
Abstract Fine root litter is a primary source of soil organic matter (SOM), which is a globally important pool of C that is responsive to climate change. We previously established that ~20 years of experimental nitrogen (N) deposition has slowed fine root decay and increased the storage of soil carbon (C; +18%) across a widespread northern hardwood forest ecosystem. However, the microbial mechanisms that have directly slowed fine root decay are unknown. Here, we show that experimental N deposition has decreased the relative abundance of Agaricales fungi (−31%) and increased that of partially ligninolytic Actinobacteria (+24%) on decaying fine roots. Moreover, experimental N deposition has increased the relative abundance of lignin‐derived compounds residing in SOM (+53%), and this biochemical response is significantly related to shifts in both fungal and bacterial community composition. Specifically, the accumulation of lignin‐derived compounds in SOM is negatively related to the relative abundance of ligninolytic
Mycena andKuehneromyces fungi, and positively related to Microbacteriaceae. Our findings suggest that by altering the composition of microbial communities on decaying fine roots such that their capacity for lignin degradation is reduced, experimental N deposition has slowed fine root litter decay, and increased the contribution of lignin‐derived compounds from fine roots to SOM. The microbial responses we observed may explain widespread findings that anthropogenic N deposition increases soil C storage in terrestrial ecosystems. More broadly, our findings directly link composition to function in soil microbial communities, and implicate compositional shifts in mediating biogeochemical processes of global significance.
