Distinct Assembly Processes and Microbial Communities Constrain Soil Organic Carbon Formation

Soil stores more carbon (C) than all vegetation and the atmosphere combined. Soil C stocks are broadly shaped by temperature, moisture, soil physical characteristics, vegetation, and microbial-mediated metabolic processes. The efficiency with which microorganisms use soil C regulates the balance between C storage in soil and the atmosphere. In this review, we discuss how microbial physiology and community assembly processes determine microbial growth rate and efficiency and, in turn, soil organic C cycling through the lens of community ecology. We introduce a conceptual framework cataloging life history (i.e., growth rate, resource acquisition, and stress tolerance) and assembly traits (i.e., competition, facilitation, and dispersal) that correspond with different growth efficiencies. We also compare how dominant mycorrhizal fungal type affects growth efficiency. We propose that further development and inclusion of specific community parameters in microbial-explicit Earth system models are needed for accurately predicting soil organic C responses to global change. Soil stores more carbon (C) than all vegetation and the atmosphere combined. Soil C stocks are broadly shaped by temperature, moisture, soil physical characteristics, vegetation, and microbial-mediated metabolic processes. The efficiency with which microorganisms use soil C regulates the balance between C storage in soil and the atmosphere. In this review, we discuss how microbial physiology and community assembly processes determine microbial growth rate and efficiency and, in turn, soil organic C cycling through the lens of community ecology. We introduce a conceptual framework cataloging life history (i.e., growth rate, resource acquisition, and stress tolerance) and assembly traits (i.e., competition, facilitation, and dispersal) that correspond with different growth efficiencies. We also compare how dominant mycorrhizal fungal type affects growth efficiency. We propose that further development and inclusion of specific community parameters in microbial-explicit Earth system models are needed for accurately predicting soil organic C responses to global change. Globally, the top two meters of soil store ∼2,500 Pg of soil organic carbon (SOC),1Köchy M. Hiederer R. Freibauer A. Global distribution of soil organic carbon—Part 1: masses and frequency distributions of SOC stocks for the tropics, permafrost regions, wetlands, and the world.Soil. 2015; 1: 351-365Crossref Scopus (107) Google Scholar whereas vegetation only holds ∼600 Pg of carbon (C).2Ciais P. Sabine C. Bala G. Bopp L. Brovkin V. Canadell J. Chhabra A. DeFries R. 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Microbiol. 2010; 8: 15-25Crossref PubMed Scopus (0) Google Scholar Since species must balance investment into growth, dispersal, stress tolerance, resource acquisition, and competitive and facilitative abilities, tradeoffs among these investments affect microbial metabolism and, in turn, SOC cycling (Figure 1). In this review, we synthesize how the assembly and life-history composition of soil microbial communities influence the production of necromass and by-products that become SOM. Since SOM is the repository for SOC, we primarily discuss SOM but address SOM and SOC throughout. Recent insights into SOM chemistry via spectroscopy and microbial assembly via molecular analyses—much of which are context specific—have not been well integrated. We argue that it is essential to better merge these areas of research in order to guide cohesive development in SOC research. At a time of unprecedented global change, it is critical to have a solid conceptual basis upon which we can predict SOC responses to different global change scenarios. Fundamentally, microbial SOM formation is an outcome of microbial growth, which is frequently represented by growth rate and efficiency. Whole soil growth efficiency is primarily modeled as the proportion of C that is incorporated into biomass versus respiration (i.e., C use efficiency), with this value ranging between <0.1 and >0.9 for individual organisms and typically between 0.25 and 0.8 for whole communities depending on community structure, substrate type, and environmental conditions.25Manzoni S. Taylor P. Richter A. Porporato A. Ågren G.I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils.New Phytol. 2012; 196: 79-91Crossref PubMed Scopus (477) Google Scholar,43Qiao Y. Wang J. Liang G. Du Z. Zhou J. Zhu C. Huang K. Zhou X. Luo Y. 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MSc thesis (University of New Hampshire).Google Scholar Across heterotrophic bacterial and fungal culture lines, growth rate and efficiency can be positively correlated,36Pold G. Domeignoz-Horta L.A. Morrison E.W. Frey S.D. Sistla S.A. DeAngelis K.M. Carbon use efficiency and its temperature sensitivity covary in soil bacteria.mBio. 2020; 11https://doi.org/10.1128/mBio.02293-19Crossref PubMed Scopus (0) Google Scholar,49Whit