Endemism and functional convergence across the North American soil mycobiome

Abstract

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.T he structure and function of ecological communities are intimately linked, such that the number and identity of species within a community often affect the key ecosystem properties of primary productivity (1), resistance and resilience to disturbance (2), and rates of nutrient cycling (3). However, understanding the extent to which structure-function relationships hold across communities and over large spatial scales continues to be a major goal of ecological research. Identifying these relationships for microbial organisms is particularly critical, because these organisms control rates of key ecosystem processes (the cycling of nitrogen, phosphorus, and carbon) (4) and directly affect the community structure of plants and animals through pathogenic or mutualistic interactions (5). As such, microbial activity is also intrinsic to Earth system models that inform citizens and policy makers of ecosystem dynamics and energy exchange between the biosphere and the atmosphere (6). As in plant communities of tropical rainforests (7), the incredible number of microbial taxa on Earth has been a challenge for understanding the link between diversity and function. Advances in DNA sequencing technology have recently allowed for a robust characterization of bacterial biogeographic patterns (8); however, to date, studies have examined structure-function relationships at a fixed scale (9-12). As a result, it is not yet clear how microbial function is linked to largescale biogeographic patterns, whether or not this link is a more reliable determinant of microbial function in global biogeochemical cycl...

Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships

“…These results support our initial hypothesis and provide direct evidence for the microbial regulation of soil processes linked to C degradation in terrestrial ecosystems. Our results suggest environmental filters are primary responsible for the assembly of soil microbial community and determine the strong differences in the community composition between different geographic regions (Fierer et al, 2013;Talbot et al, 2014). However, the functional potential of the microbial community will be driven by the selection of active taxa within different lineages.…”

“…In addition, this strong correlation also indicates that functional genes can be used to develop a gene-centric approach to integrate environmental genomics into simulation models in order to improve their predictive power and accuracy of ESMs (Reed et al, 2014). Regulatory pathways of the activity of enzymes involved in C degradation Identifying the structural-functional relationships for microbial organisms is particularly critical to determine the importance of the soil microbial community in regulating ecosystem processes, and thus there is keen interest in developing theoretical and experimental approaches to disentangle the microbial regulation of soil functions from other biotic and abiotic drivers (for example, Strickland et al, 2009;Wallenstein and Hall, 2012;Talbot et al, 2014;You et al, 2014;Wood et al, 2015). Albeit we found that functional genes were strongly related to enzyme activities, these results are correlative in nature and hence potentially non-causative.…”

“…This allows us to identify the main microbial groups driving functional genes and soil functioning, which would not have been possible by including a global diversity metric such as evenness or Shannon diversity. In these analyses, we chose soil C and pH as the explanatory variables because both have been demonstrated previously as primary factors determining not only the structure of soil microbial community (Rousk et al, 2010;You et al, 2014) but also the production of soil enzymes involved in C degradation (Talbot et al, 2014;You et al, 2014). In addition, we included the relative abundance of particular microbial groups that were previously identified to be important predictors of enzyme activities in our soil samples by RF analysis.…”

“…Processlevel analyses such as respiration and enzymatic transformation of added substrate are used as a proxy of microbial function, which gives valuable insight into overall microbial-mediated transformations in soils. However, such measurements do not provide concrete links on mechanisms, microbial functional composition and diversity that underpins processlevel differences (Reeve et al, 2010;Talbot et al, 2014;You et al, 2014). Few studies conducted at local scale have observed relationships between community composition and biochemical function of microbes in soils (Fierer et al, 2012;Talbot et al, 2014;Su et al, 2015), suggesting that the composition of microbial communities, per se, may be important.…”

“…However, such measurements do not provide concrete links on mechanisms, microbial functional composition and diversity that underpins processlevel differences (Reeve et al, 2010;Talbot et al, 2014;You et al, 2014). Few studies conducted at local scale have observed relationships between community composition and biochemical function of microbes in soils (Fierer et al, 2012;Talbot et al, 2014;Su et al, 2015), suggesting that the composition of microbial communities, per se, may be important. However, empirical evidence of microbial regulation of ecosystem processes is lacking that limits the coupling between microbial community functional traits, the environment context and the ecosystem processes.…”