Abstract
The recent application of macroecological tools and concepts has made it possible to identify consistent patterns in the distribution of microbial biodiversity, which greatly improved our understanding of the microbial world at large scales. However, the distribution of microbial functions remains largely uncharted from the macroecological point of view. Here, we used macroecological models to examine how the genes encoding the functional capabilities of microorganisms are distributed within and across soil systems. Models built using functional gene array data from 818 soil microbial communities showed that the occupancy-frequency distributions of genes were bimodal in every studied site, and that their rank-abundance distributions were best described by a lognormal model. In addition, the relationships between gene occupancy and abundance were positive in all sites. This allowed us to identify genes with high abundance and ubiquitous distribution (core) and genes with low abundance and limited spatial distribution (satellites), and to show that they encode different sets of microbial traits. Common genes encode microbial traits related to the main biogeochemical cycles (C, N, P and S) while rare genes encode traits related to adaptation to environmental stresses, such as nutrient limitation, resistance to heavy metals and degradation of xenobiotics. Overall, this study characterized for the first time the distribution of microbial functional genes within soil systems, and highlight the interest of macroecological models for understanding the functional organization of microbial systems across spatial scales.
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Acknowledgements
The authors would like to thank all the persons that contributed to sample collection and laboratory analyses. This synthesis was primarily funded by the U.S. Department of Energy (DOE), Office of Science, Office of Biological and Environmental Research’s (OBER) Systems Biology Research to Advance Sustainable Bioenergy Crop Development (DE-SC0014079), Biological Systems Research on the Role of Microbial Communities in Carbon Cycling program (DE-SC0004730, DE-SC001057, DE-SC0004601 and DE-SC0010715), by the U.S. National Science Foundation MacroSystems Biology program under the contract (NSF EF-1065844), and by the Office of the Vice President for Research at the University of Oklahoma, all to JZ. This work was also supported by the National Natural Science Foundation of China (No.31670614) to YY.
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AE developed the original concept of the study. FP, MY, FL, JF, LW, YZ, and YY provided experimental data. AE and FG performed data analyses. AE wrote the first draft of the paper with help from FP, FG, MY, YY, FL, JF, LW, YZ, and JZ.
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Escalas, A., Paula, F.S., Guilhaumon, F. et al. Macroecological distributions of gene variants highlight the functional organization of soil microbial systems. ISME J 16, 726–737 (2022). https://doi.org/10.1038/s41396-021-01120-8
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DOI: https://doi.org/10.1038/s41396-021-01120-8
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