TY - JOUR
T1 - Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity
AU - the Earth Microbiome Project 500 (EMP500) Consortium
AU - Shaffer, Justin P.
AU - Nothias, Louis Félix
AU - Thompson, Luke R.
AU - Sanders, Jon G.
AU - Salido, Rodolfo A.
AU - Couvillion, Sneha P.
AU - Brejnrod, Asker D.
AU - Lejzerowicz, Franck
AU - Haiminen, Niina
AU - Huang, Shi
AU - Lutz, Holly L.
AU - Zhu, Qiyun
AU - Martino, Cameron
AU - Morton, James T.
AU - Karthikeyan, Smruthi
AU - Nothias-Esposito, Mélissa
AU - Dührkop, Kai
AU - Böcker, Sebastian
AU - Kim, Hyun Woo
AU - Aksenov, Alexander A.
AU - Bittremieux, Wout
AU - Minich, Jeremiah J.
AU - Marotz, Clarisse
AU - Bryant, MacKenzie K.M.
AU - Sanders, Karenina
AU - Schwartz, Tara
AU - Humphrey, Greg
AU - Vásquez-Baeza, Yoshiki
AU - Tripathi, Anupriya
AU - Parida, Laxmi
AU - Carrieri, Anna Paola
AU - Beck, Kristen L.
AU - Das, Promi
AU - González, Antonio
AU - McDonald, Daniel
AU - Ladau, Joshua
AU - Karst, Søren M.
AU - Albertsen, Mads
AU - Ackermann, Gail
AU - DeReus, Jeff
AU - Thomas, Torsten
AU - Petras, Daniel
AU - Shade, Ashley
AU - Stegen, James
AU - Song, Se Jin
AU - Metz, Thomas O.
AU - Swafford, Austin D.
AU - Dorrestein, Pieter C.
AU - Jansson, Janet K.
AU - U’Ren, Jana M.
N1 - Funding Information:
We thank G. Milivenvsky, A. Møller, I. Chizhevsky, S. Kirieiev, A. Nosovsky and M. Ivanenko for logistic support with fieldwork in Ukraine; L. Goldasich and J. Toronczak for assistance with sample processing for sequencing; M. Fedarko, R. Diner, E. Wood-Charlson, S. Nayfach, D. Udwary and E. Eloe-Fadrosh for reviewing the manuscript. This work was supported in part by the Samuel Freeman Charitable Trust, US National Institute of Health (NIH) (awards 1RF1-AG058942-01, 1DP1AT010885, R01HL140976, R01DK102932, R01HL134887, U19AG063744 and U01AI124316 to R.K.), US Department of Agriculture – National Institute of Food and Agriculture (USDA-NIFA) (award 2019-67013-29137 to R.K.), the US National Science Foundation (NSF) - Center for Aerosol Impacts on Chemistry of the Environment, Crohn’s & Colitis Foundation Award (CCFA) (award 675191 to R.K.), US Department of Energy - Office of Science - Office of Biological and Environmental Research - Environmental System Science Program, Semiconductor Research Corporation and Defence Advanced Research Projects Agency (SRC/DARPA) (award GI18518 to R.K.), Department of Defense (award W81XWH-17-1-0589 to R.K.), the Office of Naval Research (ONR) (award N00014-15-1-2809 to R.K.), the Emerald Foundation (award 3022 to R.K.), IBM Research AI through the AI Horizons Network, and the Center for Microbiome Innovation. J.P.S. was supported by NIH/NIGMS IRACDA K12 GM068524. L.-F.N. was supported by the NIH (award R01-GM107550). A.D.B. was supported by the Danish Council for Independent Research (DFF) (award 9058-00025B). W.B. was supported by the Research Foundation – Flanders (12W0418N). K.D. and S.B. were supported by Deutsche Forschungsgemeinschaft (BO 1910/20 and 1910/23). P.C.D. was supported by the Gordon and Betty Moore Foundation (award GBMF7622) and the NIH (award R01-GM107550). Metabolomics analyses at Pacific Northwest National Laboratory (PNNL) were supported by the Laboratory Directed Research and Development program via the Microbiomes in Transition Initiative and performed in the Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the US Office of Biological and Environmental Research and located at PNNL. This contribution originates in part from the River Corridor Scientific Focus Area project at PNNL. PNNL is a multiprogram national laboratory operated by Battelle for the Department of Energy (DOE) under contract DE-AC05-76RLO 1830, as well as work supported by COMPASS-FME, a multi-institutional project supported by the US DOE, Office of Science, Biological and Environmental Research as part of the Environmental System Science Program. We thank Eppendorf, Illumina and Integrated DNA Technologies for in-kind support at various phases of the project.
Funding Information:
We thank G. Milivenvsky, A. Møller, I. Chizhevsky, S. Kirieiev, A. Nosovsky and M. Ivanenko for logistic support with fieldwork in Ukraine; L. Goldasich and J. Toronczak for assistance with sample processing for sequencing; M. Fedarko, R. Diner, E. Wood-Charlson, S. Nayfach, D. Udwary and E. Eloe-Fadrosh for reviewing the manuscript. This work was supported in part by the Samuel Freeman Charitable Trust, US National Institute of Health (NIH) (awards 1RF1-AG058942-01, 1DP1AT010885, R01HL140976, R01DK102932, R01HL134887, U19AG063744 and U01AI124316 to R.K.), US Department of Agriculture – National Institute of Food and Agriculture (USDA-NIFA) (award 2019-67013-29137 to R.K.), the US National Science Foundation (NSF) - Center for Aerosol Impacts on Chemistry of the Environment, Crohn’s & Colitis Foundation Award (CCFA) (award 675191 to R.K.), US Department of Energy - Office of Science - Office of Biological and Environmental Research - Environmental System Science Program, Semiconductor Research Corporation and Defence Advanced Research Projects Agency (SRC/DARPA) (award GI18518 to R.K.), Department of Defense (award W81XWH-17-1-0589 to R.K.), the Office of Naval Research (ONR) (award N00014-15-1-2809 to R.K.), the Emerald Foundation (award 3022 to R.K.), IBM Research AI through the AI Horizons Network, and the Center for Microbiome Innovation. J.P.S. was supported by NIH/NIGMS IRACDA K12 GM068524. L.-F.N. was supported by the NIH (award R01-GM107550). A.D.B. was supported by the Danish Council for Independent Research (DFF) (award 9058-00025B). W.B. was supported by the Research Foundation – Flanders (12W0418N). K.D. and S.B. were supported by Deutsche Forschungsgemeinschaft (BO 1910/20 and 1910/23). P.C.D. was supported by the Gordon and Betty Moore Foundation (award GBMF7622) and the NIH (award R01-GM107550). Metabolomics analyses at Pacific Northwest National Laboratory (PNNL) were supported by the Laboratory Directed Research and Development program via the Microbiomes in Transition Initiative and performed in the Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the US Office of Biological and Environmental Research and located at PNNL. This contribution originates in part from the River Corridor Scientific Focus Area project at PNNL. PNNL is a multiprogram national laboratory operated by Battelle for the Department of Energy (DOE) under contract DE-AC05-76RLO 1830, as well as work supported by COMPASS-FME, a multi-institutional project supported by the US DOE, Office of Science, Biological and Environmental Research as part of the Environmental System Science Program. We thank Eppendorf, Illumina and Integrated DNA Technologies for in-kind support at various phases of the project.
Publisher Copyright:
© 2022, The Author(s).
PY - 2022/12
Y1 - 2022/12
N2 - Despite advances in sequencing, lack of standardization makes comparisons across studies challenging and hampers insights into the structure and function of microbial communities across multiple habitats on a planetary scale. Here we present a multi-omics analysis of a diverse set of 880 microbial community samples collected for the Earth Microbiome Project. We include amplicon (16S, 18S, ITS) and shotgun metagenomic sequence data, and untargeted metabolomics data (liquid chromatography-tandem mass spectrometry and gas chromatography mass spectrometry). We used standardized protocols and analytical methods to characterize microbial communities, focusing on relationships and co-occurrences of microbially related metabolites and microbial taxa across environments, thus allowing us to explore diversity at extraordinary scale. In addition to a reference database for metagenomic and metabolomic data, we provide a framework for incorporating additional studies, enabling the expansion of existing knowledge in the form of an evolving community resource. We demonstrate the utility of this database by testing the hypothesis that every microbe and metabolite is everywhere but the environment selects. Our results show that metabolite diversity exhibits turnover and nestedness related to both microbial communities and the environment, whereas the relative abundances of microbially related metabolites vary and co-occur with specific microbial consortia in a habitat-specific manner. We additionally show the power of certain chemistry, in particular terpenoids, in distinguishing Earth’s environments (for example, terrestrial plant surfaces and soils, freshwater and marine animal stool), as well as that of certain microbes including Conexibacter woesei (terrestrial soils), Haloquadratum walsbyi (marine deposits) and Pantoea dispersa (terrestrial plant detritus). This Resource provides insight into the taxa and metabolites within microbial communities from diverse habitats across Earth, informing both microbial and chemical ecology, and provides a foundation and methods for multi-omics microbiome studies of hosts and the environment.
AB - Despite advances in sequencing, lack of standardization makes comparisons across studies challenging and hampers insights into the structure and function of microbial communities across multiple habitats on a planetary scale. Here we present a multi-omics analysis of a diverse set of 880 microbial community samples collected for the Earth Microbiome Project. We include amplicon (16S, 18S, ITS) and shotgun metagenomic sequence data, and untargeted metabolomics data (liquid chromatography-tandem mass spectrometry and gas chromatography mass spectrometry). We used standardized protocols and analytical methods to characterize microbial communities, focusing on relationships and co-occurrences of microbially related metabolites and microbial taxa across environments, thus allowing us to explore diversity at extraordinary scale. In addition to a reference database for metagenomic and metabolomic data, we provide a framework for incorporating additional studies, enabling the expansion of existing knowledge in the form of an evolving community resource. We demonstrate the utility of this database by testing the hypothesis that every microbe and metabolite is everywhere but the environment selects. Our results show that metabolite diversity exhibits turnover and nestedness related to both microbial communities and the environment, whereas the relative abundances of microbially related metabolites vary and co-occur with specific microbial consortia in a habitat-specific manner. We additionally show the power of certain chemistry, in particular terpenoids, in distinguishing Earth’s environments (for example, terrestrial plant surfaces and soils, freshwater and marine animal stool), as well as that of certain microbes including Conexibacter woesei (terrestrial soils), Haloquadratum walsbyi (marine deposits) and Pantoea dispersa (terrestrial plant detritus). This Resource provides insight into the taxa and metabolites within microbial communities from diverse habitats across Earth, informing both microbial and chemical ecology, and provides a foundation and methods for multi-omics microbiome studies of hosts and the environment.
UR - http://www.scopus.com/inward/record.url?scp=85142932091&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85142932091&partnerID=8YFLogxK
U2 - 10.1038/s41564-022-01266-x
DO - 10.1038/s41564-022-01266-x
M3 - Article
C2 - 36443458
AN - SCOPUS:85142932091
SN - 2058-5276
VL - 7
SP - 2128
EP - 2150
JO - Nature Microbiology
JF - Nature Microbiology
IS - 12
ER -