Microbial communities are not the easiest to manipulate experimentally in natural ecosystems. However, leaf litter—topmost layer of surface soil—is uniquely suitable to investigate the complexities of community assembly. Here, we reflect on over a decade of collaborative work to address this topic using leaf litter as a model system in Southern California ecosystems. By leveraging a number of methodological advantages of the system, we have worked to demonstrate how four processes—selection, dispersal, drift, and diversification—contribute to bacterial and fungal community assembly and ultimately impact community functioning. Although many dimensions remain to be investigated, our initial results demonstrate that both ecological and evolutionary processes occur simultaneously to influence microbial community assembly. We propose that the development of additional and experimentally tractable microbial systems will be enormously valuable to test the role of eco-evolutionary processes in natural settings and their implications in the face of rapid global change.
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Abstract Microbial communities respond to changes in environmental conditions; however, how compositional shifts affect ecosystem processes is still not well-understood and it is often assumed that different microbial communities will function equally under similar environmental conditions. We evaluated this assumption of functional redundancy using biological soil crusts (BSCs) from two arid ecosystems in Mexico with contrasting climate conditions (hot and cold deserts) following an experimental approach both in the field (reciprocal transplants) and in laboratory conditions (common garden), focusing on the community’s composition and potential for nitrogen fixation. Potential of nitrogen fixation was assessed through the acetylene reduction assay. Community composition and diversity was determined with T-RFLPs of nifH gene, high throughput sequencing of 16S rRNA gene amplicons and metagenomic libraries. BSCs tended to show higher potential nitrogen fixation rates when experiencing temperatures more similar to their native environment. Moreover, changes in potential nitrogen fixation, taxonomic and functional community composition, and diversity often depended on an interactive effect of origin of the communities and the environment they experienced. We interpret our results as legacy effects that result from ecological specialization of the BSC communities to their native environment. Overall, we present evidence of nonfunctional redundancy of BSCs in terms of nitrogen fixation.
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Abstract Recent evidence suggests that, similar to larger organisms, dispersal is a key driver of microbiome assembly; however, our understanding of the rates and taxonomic composition of microbial dispersal in natural environments is limited. Here, we characterized the rate and composition of bacteria dispersing into surface soil via three dispersal routes (from the air above the vegetation, from nearby vegetation and leaf litter near the soil surface, and from the bulk soil and litter below the top layer). We then quantified the impact of those routes on microbial community composition and functioning in the topmost litter layer. The bacterial dispersal rate onto the surface layer was low (7900 cells/cm2/day) relative to the abundance of the resident community. While bacteria dispersed through all three routes at the same rate, only dispersal from above and near the soil surface impacted microbiome composition, suggesting that the composition, not rate, of dispersal influenced community assembly. Dispersal also impacted microbiome functioning. When exposed to dispersal, leaf litter decomposed faster than when dispersal was excluded, although neither decomposition rate nor litter chemistry differed by route. Overall, we conclude that the dispersal routes transport distinct bacterial communities that differentially influence the composition of the surface soil microbiome.
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Abstract Microorganisms are the primary engines of biogeochemical processes and foundational to the provisioning of ecosystem services to human society. Free‐living microbial communities (microbiomes) and their functioning are now known to be highly sensitive to environmental change. Given microorganisms' capacity for rapid evolution, evolutionary processes could play a role in this response. Currently, however, few models of biogeochemical processes explicitly consider how microbial evolution will affect biogeochemical responses to environmental change. Here, we propose a conceptual framework for explicitly integrating evolution into microbiome–functioning relationships. We consider how microbiomes respond simultaneously to environmental change via four interrelated processes that affect overall microbiome functioning (physiological acclimation, demography, dispersal and evolution). Recent evidence in both the laboratory and the field suggests that ecological and evolutionary dynamics occur simultaneously within microbiomes; however, the implications for biogeochemistry under environmental change will depend on the timescales over which these processes contribute to a microbiome's response. Over the long term, evolution may play an increasingly important role for microbially driven biogeochemical responses to environmental change, particularly to conditions without recent historical precedent.
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Bacteria and fungi drive decomposition, a fundamental process in the carbon cycle, yet the importance of microbial community composition for decomposition remains elusive. Here, we used an 18-month reciprocal transplant experiment along a climate gradient in Southern California to disentangle the effects of the microbial community versus the environment on decomposition. Specifically, we tested whether the decomposition response to climate change depends on the microbial community. We inoculated microbial decomposers from each site onto a common, irradiated leaf litter within “microbial cages” that prevent microbial exchange with the environment. We characterized fungal and bacterial composition and abundance over time and investigated the functional consequences through litter mass loss and chemistry. After 12 months, microbial communities altered both decomposition rate and litter chemistry. Further, the functional measurements depended on an interaction between the community and its climate in a manner not predicted by current theory. Moreover, microbial ecologists have traditionally considered fungi to be the primary agents of decomposition and for bacteria to play a minor role. Our results indicate that not only does climate change and transplantation have differential legacy effects among bacteria and fungi, but also that bacterial communities might be less functionally redundant than fungi with regards to decomposition. Thus, it may be time to reevaluate both the role of microbial community composition in its decomposition response to climate and the relative roles of bacterial and fungal communities in decomposition.
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Summary The high diversity of soil bacteria is attributed to the spatial complexity of soil systems, where habitat heterogeneity promotes niche partitioning among bacterial taxa. This premise remains challenging to test, however, as it requires quantifying the traits of closely related soil bacteria and relating these traits to bacterial abundances and geographic distributions. Here, we sought to investigate whether the widespread soil taxon
Curtobacterium consists of multiple coexisting ecotypes with differential geographic distributions. We isolatedCurtobacterium strains from six sites along a climate gradient and assayed four functional traits that may contribute to niche partitioning in leaf litter, the top layer of soil. Our results revealed that cultured isolates separated into fine‐scale genetic clusters that reflected distinct suites of phenotypic traits, denoting the existence of multiple ecotypes. We then quantified the distribution ofCurtobacterium by analysing metagenomic data collected across the gradient over 18 months. Six abundant ecotypes were observed with differential abundances along the gradient, suggesting fine‐scale niche partitioning. However, we could not clearly explain observed geographic distributions of ecotypes by relating their traits to environmental variables. Thus, while we can resolve soil bacterial ecotypes, the traits delineating their distinct niches in the environment remain unclear.