Macroecological distributions of gene variants highlight the functional organization of soil microbial systems

Escalas, Arthur; Paula, Fabiana S.; Guilhaumon, François; Yuan, Mengting; Yang, Yunfeng; Wu, Linwei; Liu, Feifei; Feng, Jiaje; Zhang, Yuguang; Zhou, Jizhong

doi:10.1038/s41396-021-01120-8

Title: Macroecological distributions of gene variants highlight the functional organization of soil microbial systems

Journal Article · Mon Sep 27 00:00:00 EDT 2021 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-021-01120-8· OSTI ID:2280704

; Paula, Fabiana S.; Guilhaumon, François;

;

; Wu, Linwei;

; Feng, Jiaje;

;

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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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Natural Science Foundation of China (NSFC)

Grant/Contract Number:: SC0014079; AC02-05CH11231; SC0004730; SC001057; SC0004601; SC0010715; 1065844; 31670614

OSTI ID:: 2280704

Alternate ID(s):: OSTI ID: 1901551

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Vol. 16 Journal Issue: 3; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (83)

Interactions in the microbiome: communities of organisms and communities of genes Boon, Eva; Meehan, Conor J.; Whidden, Chris FEMS Microbiology Reviews, Vol. 38, Issue 1 https://doi.org/10.1111/1574-6976.12035	journal	January 2014
Microbial functional diversity: From concepts to applications Escalas, Arthur; Hale, Lauren; Voordeckers, James W. Ecology and Evolution, Vol. 9, Issue 20 https://doi.org/10.1002/ece3.5670	journal	September 2019
Patterns of Rare and Abundant Marine Microbial Eukaryotes Logares, Ramiro; Audic, Stéphane; Bass, David Current Biology, Vol. 24, Issue 8 https://doi.org/10.1016/j.cub.2014.02.050	journal	April 2014
Explaining abundance-occupancy relationships in specialists and generalists: a case study on aquatic macroinvertebrates in standing waters Verberk, Wilco C. E. P.; van der Velde, Gerard; Esselink, Hans Journal of Animal Ecology, Vol. 79, Issue 3 https://doi.org/10.1111/j.1365-2656.2010.01660.x	journal	May 2010
Ecology and exploration of the rare biosphere Lynch, Michael D. J.; Neufeld, Josh D. Nature Reviews Microbiology, Vol. 13, Issue 4 https://doi.org/10.1038/nrmicro3400	journal	March 2015
Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity Shade, A.; Jones, S. E.; Caporaso, J. G. mBio, Vol. 5, Issue 4 https://doi.org/10.1128/mBio.01371-14	journal	July 2014
Oligotrophs versus copiotrophs Koch, Arthur L. BioEssays, Vol. 23, Issue 7 https://doi.org/10.1002/bies.1091	journal	January 2001
Global diversity and biogeography of bacterial communities in wastewater treatment plants Wu, Linwei; Ning, Daliang; Zhang, Bing Nature Microbiology, Vol. 4, Issue 7 https://doi.org/10.1038/s41564-019-0426-5	journal	May 2019
The importance of resolving biogeographic patterns of microbial microdiversity Chase, Alexander B.; Martiny, Jennifer BH Microbiology Australia, Vol. 39, Issue 1 https://doi.org/10.1071/MA18003	journal	January 2018
Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance Wertz, Sophie; Degrange, Valérie; Prosser, James I. Environmental Microbiology, Vol. 9, Issue 9 https://doi.org/10.1111/j.1462-2920.2007.01335.x	journal	September 2007
Bacterial Community Structure at the Microscale in Two Different Soils Michelland, Rory; Thioulouse, Jean; Kyselková, Martina Microbial Ecology, Vol. 72, Issue 3 https://doi.org/10.1007/s00248-016-0810-0	journal	July 2016
Strain/Species-Specific Probe Design for Microbial Identification Microarrays Tu, Q.; He, Z.; Deng, Y. Applied and Environmental Microbiology, Vol. 79, Issue 16 https://doi.org/10.1128/AEM.01124-13	journal	June 2013
A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa: Weak response of rare bacteria to abiotic change Kurm, Viola; Geisen, Stefan; Gera Hol, Wilhelmina H. Environmental Microbiology, Vol. 21, Issue 2 https://doi.org/10.1111/1462-2920.14492	journal	December 2018
GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes He, Zhili; Gentry, Terry J.; Schadt, Christopher W. The ISME Journal, Vol. 1, Issue 1 https://doi.org/10.1038/ismej.2007.2	journal	May 2007
High-Throughput Metagenomic Technologies for Complex Microbial Community Analysis: Open and Closed Formats Zhou, Jizhong; He, Zhili; Yang, Yunfeng mBio, Vol. 6, Issue 1 https://doi.org/10.1128/mBio.02288-14	journal	January 2015
Temporal patterns of rarity provide a more complete view of microbial diversity Shade, Ashley; Gilbert, Jack A. Trends in Microbiology, Vol. 23, Issue 6 https://doi.org/10.1016/j.tim.2015.01.007	journal	June 2015
Soil Microbial Community Responses to a Decade of Warming as Revealed by Comparative Metagenomics Luo, Chengwei; Rodriguez-R, Luis M.; Johnston, Eric R. Applied and Environmental Microbiology, Vol. 80, Issue 5 https://doi.org/10.1128/AEM.03712-13	journal	December 2013
Soil-Borne Microbiome: Linking Diversity to Function Mendes, Lucas W.; Tsai, Siu M.; Navarrete, Acácio A. Microbial Ecology, Vol. 70, Issue 1 https://doi.org/10.1007/s00248-014-0559-2	journal	January 2015
Benefits of plant diversity to ecosystems: immediate, filter and founder effects Grime, J. P. Journal of Ecology, Vol. 86, Issue 6 https://doi.org/10.1046/j.1365-2745.1998.00306.x	journal	December 1998
Abundance-occupancy relationships in deep sea wood fall communities Webb, Thomas J.; Barry, James P.; McClain, Craig R. Ecography, Vol. 40, Issue 11 https://doi.org/10.1111/ecog.02618	journal	January 2017
Selection of optimal oligonucleotide probes for microarrays using multiple criteria, global alignment and parameter estimation Li, X. Nucleic Acids Research, Vol. 33, Issue 19 https://doi.org/10.1093/nar/gki914	journal	October 2005
Do microbes have macroecology? Large-scale patterns in the diversity and distribution of marine benthic ciliates: Do microbes have macroecology? Azovsky, Andrey; Mazei, Yuri Global Ecology and Biogeography, Vol. 22, Issue 2 https://doi.org/10.1111/j.1466-8238.2012.00776.x	journal	June 2012
Bimodality in Occurrence Classes: A Direct Consequence of Lognormal or Logarithmic Series Distribution of Abundances: A Numerical Experimentation Papp, László; Izsák, János; Papp, Laszlo Oikos, Vol. 79, Issue 1 https://doi.org/10.2307/3546107	journal	May 1997
The microbial gene diversity along an elevation gradient of the Tibetan grassland Yang, Yunfeng; Gao, Ying; Wang, Shiping The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.146	journal	August 2013
Abundance-occupancy relationships Gaston, Kevin J.; Blackburn, Tim M.; Greenwood, Jeremy J. D. Journal of Applied Ecology, Vol. 37, Issue s1 https://doi.org/10.1046/j.1365-2664.2000.00485.x	journal	September 2000
Abundance–occupancy patterns in a riverine fish assemblage Miranda, Leandro E.; Killgore, Kenneth J. Freshwater Biology, Vol. 64, Issue 12 https://doi.org/10.1111/fwb.13408	journal	October 2019
Rare taxa have potential to make metabolic contributions in enhanced biological phosphorus removal ecosystems: EBPR microbiome activity and dynamics Lawson, Christopher E.; Strachan, Blake J.; Hanson, Niels W. Environmental Microbiology, Vol. 17, Issue 12 https://doi.org/10.1111/1462-2920.12875	journal	May 2015
Reproducibility and quantitation of amplicon sequencing-based detection Zhou, Jizhong; Wu, Liyou; Deng, Ye The ISME Journal, Vol. 5, Issue 8 https://doi.org/10.1038/ismej.2011.11	journal	February 2011
Soil bacterial diversity patterns and drivers along an elevational gradient on Shennongjia Mountain, China: Soil bacterial elevational pattern Zhang, Yuguang; Cong, Jing; Lu, Hui Microbial Biotechnology, Vol. 8, Issue 4 https://doi.org/10.1111/1751-7915.12288	journal	May 2015
Functional Redundancy Supports Biodiversity and Ecosystem Function in a Closed and Constant Environment Wohl, Debra L.; Arora, Satyam; Gladstone, Jessica R. Ecology, Vol. 85, Issue 6 https://doi.org/10.1890/03-3050	journal	June 2004
GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity He, Zhili; Deng, Ye; Van Nostrand, Joy D. The ISME Journal, Vol. 4, Issue 9 https://doi.org/10.1038/ismej.2010.46	journal	April 2010
Abundance determines the functional role of bacterial phylotypes in complex communities Rivett, Damian W.; Bell, Thomas Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0180-0	journal	June 2018
Variations on a theme: sources of heterogeneity in the form of the interspecific relationship between abundance and distribution Blackburn, Tim M.; Cassey, Phillip; Gaston, Kevin J. Journal of Animal Ecology, Vol. 75, Issue 6 https://doi.org/10.1111/j.1365-2656.2006.01167.x	journal	November 2006
Microbial macroecology: In search of mechanisms governing microbial biogeographic patterns Xu, Xiaofeng; Wang, Nannan; Lipson, David Global Ecology and Biogeography, Vol. 29, Issue 11 https://doi.org/10.1111/geb.13162	journal	August 2020
Determination of the Core of a Minimal Bacterial Gene Set Gil, R.; Silva, F. J.; Pereto, J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 3 https://doi.org/10.1128/MMBR.68.3.518-537.2004	journal	September 2004
Species abundance distributions and richness estimations in fungal metagenomics - lessons learned from community ecology: COMMUNITY ECOLOGY IN FUNGAL METAGENOMICS Unterseher, Martin; Jumpponen, Ari; ÖPik, Maarja Molecular Ecology, Vol. 20, Issue 2 https://doi.org/10.1111/j.1365-294X.2010.04948.x	journal	December 2010
The Rare Bacterial Biosphere Pedrós-Alió, Carlos Annual Review of Marine Science, Vol. 4, Issue 1 https://doi.org/10.1146/annurev-marine-120710-100948	journal	January 2012
Permafrost thaw and soil moisture driving CO ₂ and CH ₄ release from upland tundra Natali, Susan M.; Schuur, Edward A. G.; Mauritz, Marguerite Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 3 https://doi.org/10.1002/2014JG002872	journal	March 2015
Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers Lindh, Markus V.; Sjöstedt, Johanna; Ekstam, Börje Environmental Microbiology, Vol. 19, Issue 3 https://doi.org/10.1111/1462-2920.13650	journal	February 2017
Dynamics of distribution in animal communities: Theory and analysis Tokeshi, Mutsunori Population Ecology, Vol. 34, Issue 2 https://doi.org/10.1007/BF02514796	journal	December 1992
Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage Fillol, Mireia; Auguet, Jean-Christophe; Casamayor, Emilio O. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.143	journal	August 2015
Macroecology to Unite All Life, Large and Small Shade, Ashley; Dunn, Robert R.; Blowes, Shane A. Trends in Ecology & Evolution, Vol. 33, Issue 10 https://doi.org/10.1016/j.tree.2018.08.005	journal	October 2018
Microbial Ecology: Finding Structure in the Rare Biosphere Bachy, Charles; Worden, Alexandra Z. Current Biology, Vol. 24, Issue 8 https://doi.org/10.1016/j.cub.2014.03.029	journal	April 2014
A communal catalogue reveals Earth’s multiscale microbial diversity Thompson, Luke R.; Sanders, Jon G.; McDonald, Daniel Nature, Vol. 551, Issue 7681 https://doi.org/10.1038/nature24621	journal	November 2017
Relating genomic characteristics to environmental preferences and ubiquity in different microbial taxa Cobo-Simón, Marta; Tamames, Javier BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3888-y	journal	June 2017
Niche breadth predicts geographical range size: a general ecological pattern Slatyer, Rachel A.; Hirst, Megan; Sexton, Jason P. Ecology Letters, Vol. 16, Issue 8 https://doi.org/10.1111/ele.12140	journal	June 2013
Disentangling the mechanisms shaping the surface ocean microbiota Logares, Ramiro; Deutschmann, Ina M.; Junger, Pedro C. Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00827-8	journal	April 2020
Function and functional redundancy in microbial systems Louca, Stilianos; Polz, Martin F.; Mazel, Florent Nature Ecology & Evolution, Vol. 2, Issue 6 https://doi.org/10.1038/s41559-018-0519-1	journal	April 2018
Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland Yang, Yunfeng; Wu, Linwei; Lin, Qiaoyan Global Change Biology, Vol. 19, Issue 2 https://doi.org/10.1111/gcb.12065	journal	November 2012
Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities Rodrigues, J. L. M.; Pellizari, V. H.; Mueller, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 3 https://doi.org/10.1073/pnas.1220608110	journal	December 2012
Where less may be more: how the rare biosphere pulls ecosystems strings Jousset, Alexandre; Bienhold, Christina; Chatzinotas, Antonis The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2016.174	journal	January 2017
Understanding the role of species dynamics in abundance-occupancy relationships Buckley, Hannah L.; Freckleton, Robert P. Journal of Ecology, Vol. 98, Issue 3 https://doi.org/10.1111/j.1365-2745.2010.01650.x	journal	May 2010
Using the taxon-specific genes for the taxonomic classification of bacterial genomes Gupta, Ankit; Sharma, Vineet K. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1542-0	journal	May 2015
Resuscitation of the rare biosphere contributes to pulses of ecosystem activity Aanderud, Zachary T.; Jones, Stuart E.; Fierer, Noah Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00024	journal	January 2015
Structure and function of the global ocean microbiome Sunagawa, S.; Coelho, L. P.; Chaffron, S. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1261359	journal	May 2015
Using network analysis to explore co-occurrence patterns in soil microbial communities Barberán, Albert; Bates, Scott T.; Casamayor, Emilio O. The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.119	journal	September 2011
Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes Polz, Martin F.; Hunt, Dana E.; Preheim, Sarah P. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1475 https://doi.org/10.1098/rstb.2006.1928	journal	October 2006
Seeing the forest for the genes: using metagenomics to infer the aggregated traits of microbial communities Fierer, Noah; BarberÃ¡n, Albert; Laughlin, Daniel C. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00614	journal	November 2014
Lifestyles of rarity: understanding heterotrophic strategies to inform the ecology of the microbial rare biosphere Newton, Rj; Shade, A. Aquatic Microbial Ecology, Vol. 78, Issue 1 https://doi.org/10.3354/ame01801	journal	December 2016
Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition Reich, Peter B.; Knops, Jean; Tilman, David Nature, Vol. 410, Issue 6830 https://doi.org/10.1038/35071062	journal	April 2001
Functional diversity and redundancy across fish gut, sediment and water bacterial communities Escalas, Arthur; Troussellier, Marc; Yuan, Tong Environmental Microbiology, Vol. 19, Issue 8 https://doi.org/10.1111/1462-2920.13822	journal	July 2017
Dynamics of Regional Distribution: The Core and Satellite Species Hypothesis Hanski, Ilkka Oikos, Vol. 38, Issue 2 https://doi.org/10.2307/3544021	journal	March 1982
Ubiquitous abundance distribution of non-dominant plankton across the global ocean Ser-Giacomi, Enrico; Zinger, Lucie; Malviya, Shruti Nature Ecology & Evolution, Vol. 2, Issue 8 https://doi.org/10.1038/s41559-018-0587-2	journal	June 2018
Maintenance of soil functioning following erosion of microbial diversity Wertz, Sophie; Degrange, Valérie; Prosser, James I. Environmental Microbiology, Vol. 8, Issue 12 https://doi.org/10.1111/j.1462-2920.2006.01098.x	journal	December 2006
Occupancy frequency distributions: patterns, artefacts and mechanisms McGEOCH, Melodie A.; Gaston, Kevin J. Biological Reviews of the Cambridge Philosophical Society, Vol. 77, Issue 3 https://doi.org/10.1017/S1464793101005887	journal	August 2002
The importance of neutral and niche processes for bacterial community assembly differs between habitat generalists and specialists Liao, Jingqiu; Cao, Xiaofeng; Zhao, Lei FEMS Microbiology Ecology, Vol. 92, Issue 11 https://doi.org/10.1093/femsec/fiw174	journal	August 2016
Temporally Stable Species Occupancy Frequency Distribution and Abundance–Occupancy Relationship Patterns in Urban Wintering Bird Assemblages Suhonen, Jukka; Jokimäki, Jukka Frontiers in Ecology and Evolution, Vol. 7 https://doi.org/10.3389/fevo.2019.00129	journal	April 2019
Bacteria Are Smartphones and Mobile Genes Are Apps Young, J. Peter W. Trends in Microbiology, Vol. 24, Issue 12 https://doi.org/10.1016/j.tim.2016.09.002	journal	December 2016
Scaling laws predict global microbial diversity Locey, Kenneth J.; Lennon, Jay T. Proceedings of the National Academy of Sciences, Vol. 113, Issue 21 https://doi.org/10.1073/pnas.1521291113	journal	May 2016
Microbial macroecology: highly structured prokaryotic soil assemblages in a tropical deciduous forest: Prokaryotic macroecology Noguez, Ana M.; Arita, Héctor T.; Escalante, Ana E. Global Ecology and Biogeography, Vol. 14, Issue 3 https://doi.org/10.1111/j.1466-822X.2005.00156.x	journal	May 2005
GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis Tu, Qichao; Yu, Hao; He, Zhili Molecular Ecology Resources https://doi.org/10.1111/1755-0998.12239	journal	March 2014
Life in the slow lane Hofer, Ursula Nature Reviews Microbiology, Vol. 17, Issue 5 https://doi.org/10.1038/s41579-019-0176-7	journal	March 2019
Resistance and resilience of microbial communities - temporal and spatial insurance against perturbations: Resistance and resilience of microbial communities Baho, Didier L.; Peter, Hannes; Tranvik, Lars J. Environmental Microbiology, Vol. 14, Issue 9 https://doi.org/10.1111/j.1462-2920.2012.02754.x	journal	April 2012
Response of Core Microbial Consortia to Chronic Hydrocarbon Contaminations in Coastal Sediment Habitats Jeanbille, Mathilde; Gury, Jérôme; Duran, Robert Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01637	journal	October 2016
Macroecological patterns of marine bacteria on a global scale Amend, Anthony S.; Oliver, Tom A.; Amaral-Zettler, Linda A. Journal of Biogeography, Vol. 40, Issue 4 https://doi.org/10.1111/jbi.12034	journal	November 2012
The microbial contribution to macroecology Barberán, Albert Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00203	journal	January 2014
Functional Gene Array-Based Ultrasensitive and Quantitative Detection of Microbial Populations in Complex Communities Shi, Zhou; Yin, Huaqun; Van Nostrand, Joy D. mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/mSystems.00296-19	journal	June 2019
Spatio-Temporal Variation of Core and Satellite Arbuscular Mycorrhizal Fungus Communities in Miscanthus giganteus Barnes, Christopher J.; Burns, Caitlin A.; van der Gast, Christopher J. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01278	journal	August 2016
Explaining the excess of rare species in natural species abundance distributions Magurran, Anne E.; Henderson, Peter A. Nature, Vol. 422, Issue 6933 https://doi.org/10.1038/nature01547	journal	April 2003
Microarray-Based Analysis of Subnanogram Quantities of Microbial Community DNAs by Using Whole-Community Genome Amplification Wu, L.; Liu, X.; Schadt, C. W. Applied and Environmental Microbiology, Vol. 72, Issue 7 https://doi.org/10.1128/AEM.02738-05	journal	July 2006
A macroecological theory of microbial biodiversity Shoemaker, William R.; Locey, Kenneth J.; Lennon, Jay T. Nature Ecology & Evolution, Vol. 1, Issue 5 https://doi.org/10.1038/s41559-017-0107	journal	April 2017
Land use change alters functional gene diversity, composition and abundance in Amazon forest soil microbial communities Paula, Fabiana S.; Rodrigues, Jorge L. M.; Zhou, Jizhong Molecular Ecology, Vol. 23, Issue 12 https://doi.org/10.1111/mec.12786	journal	June 2014
The physiology of growth arrest: uniting molecular and environmental microbiology Bergkessel, Megan; Basta, David W.; Newman, Dianne K. Nature Reviews Microbiology, Vol. 14, Issue 9 https://doi.org/10.1038/nrmicro.2016.107	journal	August 2016

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Title: Macroecological distributions of gene variants highlight the functional organization of soil microbial systems

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