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Title: Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity

Abstract

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-specificmore » 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.« less

Authors:
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Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Defense Advanced Research Projects Agency (DARPA); USDOD; US Department of the Navy, Office of Naval Research (ONR); USDOE Laboratory Directed Research and Development (LDRD) Program
Contributing Org.:
Earth Microbiome Project 500 (EMP500) Consortium
OSTI Identifier:
1915277
Report Number(s):
PNNL-SA-174662
Journal ID: ISSN 2058-5276
Grant/Contract Number:  
AC05-76RL01830; GI18518; W81XWH-17-1-0589; N00014-15-1-2809
Resource Type:
Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 7; Journal Issue: 12; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; chemical ecology; cheminformatics; metabolomics; microbial ecology; next-generation sequencing

Citation Formats

Shaffer, Justin P., Nothias, Louis-Félix, Thompson, Luke R., Sanders, Jon G., Salido, Rodolfo A., Couvillion, Sneha P., Brejnrod, Asker D., Lejzerowicz, Franck, Haiminen, Niina, Huang, Shi, Lutz, Holly L., Zhu, Qiyun, Martino, Cameron, Morton, James T., Karthikeyan, Smruthi, Nothias-Esposito, Mélissa, Dührkop, Kai, Böcker, Sebastian, Kim, Hyun Woo, Aksenov, Alexander A., Bittremieux, Wout, Minich, Jeremiah J., Marotz, Clarisse, Bryant, MacKenzie M., Sanders, Karenina, Schwartz, Tara, Humphrey, Greg, Vásquez-Baeza, Yoshiki, Tripathi, Anupriya, Parida, Laxmi, Carrieri, Anna Paola, Beck, Kristen L., Das, Promi, González, Antonio, McDonald, Daniel, Ladau, Joshua, Karst, Søren M., Albertsen, Mads, Ackermann, Gail, DeReus, Jeff, Thomas, Torsten, Petras, Daniel, Shade, Ashley, Stegen, James, Song, Se Jin, Metz, Thomas O., Swafford, Austin D., Dorrestein, Pieter C., Jansson, Janet K., Gilbert, Jack A., Knight, Rob, Angenant, Lars T., Berry, Alison M., Bittleston, Leonora S., Bowen, Jennifer L., Chavarría, Max, Cowan, Don A., Distel, Dan, Girguis, Peter R., Huerta-Cepas, Jaime, Jensen, Paul R., Jiang, Lingjing, King, Gary M., Lavrinienko, Anton, MacRae-Crerar, Aurora, Makhalanyane, Thulani P., Mappes, Tapio, Marzinelli, Ezequiel M., Mayer, Gregory, McMahon, Katherine D., Metcalf, Jessica L., Miyake, Sou, Mousseau, Timothy A., Murillo-Cruz, Catalina, Myrold, David, Palenik, Brian, Pinto-Tomás, Adrián A., Porazinska, Dorota L., Ramond, Jean-Baptiste, Rowher, Forest, RoyChowdhury, Taniya, Sandin, Stuart A., Schmidt, Steven K., Seedorf, Henning, Shade, Ashley, Shipway, J. Reuben, Smith, Jennifer E., Stegen, James, Stewart, Frank J., Tait, Karen, Thomas, Torsten, Tucker, Yael, U’Ren, Jana M., Watts, Phillip C., Webster, Nicole S., Zaneveld, Jesse R., and Zhang, Shan. Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity. United States: N. p., 2022. Web. doi:10.1038/s41564-022-01266-x.
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Shaffer, Justin P., Nothias, Louis-Félix, Thompson, Luke R., Sanders, Jon G., Salido, Rodolfo A., Couvillion, Sneha P., Brejnrod, Asker D., Lejzerowicz, Franck, Haiminen, Niina, Huang, Shi, Lutz, Holly L., Zhu, Qiyun, Martino, Cameron, Morton, James T., Karthikeyan, Smruthi, Nothias-Esposito, Mélissa, Dührkop, Kai, Böcker, Sebastian, Kim, Hyun Woo, Aksenov, Alexander A., Bittremieux, Wout, Minich, Jeremiah J., Marotz, Clarisse, Bryant, MacKenzie M., Sanders, Karenina, Schwartz, Tara, Humphrey, Greg, Vásquez-Baeza, Yoshiki, Tripathi, Anupriya, Parida, Laxmi, Carrieri, Anna Paola, Beck, Kristen L., Das, Promi, González, Antonio, McDonald, Daniel, Ladau, Joshua, Karst, Søren M., Albertsen, Mads, Ackermann, Gail, DeReus, Jeff, Thomas, Torsten, Petras, Daniel, Shade, Ashley, Stegen, James, Song, Se Jin, Metz, Thomas O., Swafford, Austin D., Dorrestein, Pieter C., Jansson, Janet K., Gilbert, Jack A., Knight, Rob, Angenant, Lars T., Berry, Alison M., Bittleston, Leonora S., Bowen, Jennifer L., Chavarría, Max, Cowan, Don A., Distel, Dan, Girguis, Peter R., Huerta-Cepas, Jaime, Jensen, Paul R., Jiang, Lingjing, King, Gary M., Lavrinienko, Anton, MacRae-Crerar, Aurora, Makhalanyane, Thulani P., Mappes, Tapio, Marzinelli, Ezequiel M., Mayer, Gregory, McMahon, Katherine D., Metcalf, Jessica L., Miyake, Sou, Mousseau, Timothy A., Murillo-Cruz, Catalina, Myrold, David, Palenik, Brian, Pinto-Tomás, Adrián A., Porazinska, Dorota L., Ramond, Jean-Baptiste, Rowher, Forest, RoyChowdhury, Taniya, Sandin, Stuart A., Schmidt, Steven K., Seedorf, Henning, Shade, Ashley, Shipway, J. Reuben, Smith, Jennifer E., Stegen, James, Stewart, Frank J., Tait, Karen, Thomas, Torsten, Tucker, Yael, U’Ren, Jana M., Watts, Phillip C., Webster, Nicole S., Zaneveld, Jesse R., & Zhang, Shan. Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity. United States. https://doi.org/10.1038/s41564-022-01266-x
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Shaffer, Justin P., Nothias, Louis-Félix, Thompson, Luke R., Sanders, Jon G., Salido, Rodolfo A., Couvillion, Sneha P., Brejnrod, Asker D., Lejzerowicz, Franck, Haiminen, Niina, Huang, Shi, Lutz, Holly L., Zhu, Qiyun, Martino, Cameron, Morton, James T., Karthikeyan, Smruthi, Nothias-Esposito, Mélissa, Dührkop, Kai, Böcker, Sebastian, Kim, Hyun Woo, Aksenov, Alexander A., Bittremieux, Wout, Minich, Jeremiah J., Marotz, Clarisse, Bryant, MacKenzie M., Sanders, Karenina, Schwartz, Tara, Humphrey, Greg, Vásquez-Baeza, Yoshiki, Tripathi, Anupriya, Parida, Laxmi, Carrieri, Anna Paola, Beck, Kristen L., Das, Promi, González, Antonio, McDonald, Daniel, Ladau, Joshua, Karst, Søren M., Albertsen, Mads, Ackermann, Gail, DeReus, Jeff, Thomas, Torsten, Petras, Daniel, Shade, Ashley, Stegen, James, Song, Se Jin, Metz, Thomas O., Swafford, Austin D., Dorrestein, Pieter C., Jansson, Janet K., Gilbert, Jack A., Knight, Rob, Angenant, Lars T., Berry, Alison M., Bittleston, Leonora S., Bowen, Jennifer L., Chavarría, Max, Cowan, Don A., Distel, Dan, Girguis, Peter R., Huerta-Cepas, Jaime, Jensen, Paul R., Jiang, Lingjing, King, Gary M., Lavrinienko, Anton, MacRae-Crerar, Aurora, Makhalanyane, Thulani P., Mappes, Tapio, Marzinelli, Ezequiel M., Mayer, Gregory, McMahon, Katherine D., Metcalf, Jessica L., Miyake, Sou, Mousseau, Timothy A., Murillo-Cruz, Catalina, Myrold, David, Palenik, Brian, Pinto-Tomás, Adrián A., Porazinska, Dorota L., Ramond, Jean-Baptiste, Rowher, Forest, RoyChowdhury, Taniya, Sandin, Stuart A., Schmidt, Steven K., Seedorf, Henning, Shade, Ashley, Shipway, J. Reuben, Smith, Jennifer E., Stegen, James, Stewart, Frank J., Tait, Karen, Thomas, Torsten, Tucker, Yael, U’Ren, Jana M., Watts, Phillip C., Webster, Nicole S., Zaneveld, Jesse R., and Zhang, Shan. Mon . "Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity". United States. https://doi.org/10.1038/s41564-022-01266-x. https://www.osti.gov/servlets/purl/1915277.
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@article{osti_1915277,
title = {Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity},
author = {Shaffer, Justin P. and Nothias, Louis-Félix and Thompson, Luke R. and Sanders, Jon G. and Salido, Rodolfo A. and Couvillion, Sneha P. and Brejnrod, Asker D. and Lejzerowicz, Franck and Haiminen, Niina and Huang, Shi and Lutz, Holly L. and Zhu, Qiyun and Martino, Cameron and Morton, James T. and Karthikeyan, Smruthi and Nothias-Esposito, Mélissa and Dührkop, Kai and Böcker, Sebastian and Kim, Hyun Woo and Aksenov, Alexander A. and Bittremieux, Wout and Minich, Jeremiah J. and Marotz, Clarisse and Bryant, MacKenzie M. and Sanders, Karenina and Schwartz, Tara and Humphrey, Greg and Vásquez-Baeza, Yoshiki and Tripathi, Anupriya and Parida, Laxmi and Carrieri, Anna Paola and Beck, Kristen L. and Das, Promi and González, Antonio and McDonald, Daniel and Ladau, Joshua and Karst, Søren M. and Albertsen, Mads and Ackermann, Gail and DeReus, Jeff and Thomas, Torsten and Petras, Daniel and Shade, Ashley and Stegen, James and Song, Se Jin and Metz, Thomas O. and Swafford, Austin D. and Dorrestein, Pieter C. and Jansson, Janet K. and Gilbert, Jack A. and Knight, Rob and Angenant, Lars T. and Berry, Alison M. and Bittleston, Leonora S. and Bowen, Jennifer L. and Chavarría, Max and Cowan, Don A. and Distel, Dan and Girguis, Peter R. and Huerta-Cepas, Jaime and Jensen, Paul R. and Jiang, Lingjing and King, Gary M. and Lavrinienko, Anton and MacRae-Crerar, Aurora and Makhalanyane, Thulani P. and Mappes, Tapio and Marzinelli, Ezequiel M. and Mayer, Gregory and McMahon, Katherine D. and Metcalf, Jessica L. and Miyake, Sou and Mousseau, Timothy A. and Murillo-Cruz, Catalina and Myrold, David and Palenik, Brian and Pinto-Tomás, Adrián A. and Porazinska, Dorota L. and Ramond, Jean-Baptiste and Rowher, Forest and RoyChowdhury, Taniya and Sandin, Stuart A. and Schmidt, Steven K. and Seedorf, Henning and Shade, Ashley and Shipway, J. Reuben and Smith, Jennifer E. and Stegen, James and Stewart, Frank J. and Tait, Karen and Thomas, Torsten and Tucker, Yael and U’Ren, Jana M. and Watts, Phillip C. and Webster, Nicole S. and Zaneveld, Jesse R. and Zhang, Shan},
abstractNote = {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.},
doi = {10.1038/s41564-022-01266-x},
journal = {Nature Microbiology},
number = 12,
volume = 7,
place = {United States},
year = {Mon Nov 28 00:00:00 EST 2022},
month = {Mon Nov 28 00:00:00 EST 2022}
}
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High-accuracy long-read amplicon sequences using unique molecular identifiers with Nanopore or PacBio sequencing
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Uncovering the biosynthetic potential of rare metagenomic DNA using co-occurrence network analysis of targeted sequences
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Fecal Microbiota Transplant for Treatment of Clostridium difficile Infection in Immunocompromised Patients
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Intermittent Hypoxia and Hypercapnia Alter Diurnal Rhythms of Luminal Gut Microbiome and Metabolome
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The Integrative Human Microbiome Project
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Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use
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Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking
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VSEARCH: a versatile open source tool for metagenomics
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Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
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A Novel Sparse Compositional Technique Reveals Microbial Perturbations
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Specialized microbial metabolites: functions and origins
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Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin
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Measuring fractions of beta diversity and their relationships to nestedness: a theoretical and empirical comparison of novel approaches
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A meta-analysis study of the robustness and universality of gut microbiome-metabolome associations
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Quantifying and Understanding Well-to-Well Contamination in Microbiome Research
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SIRIUS: decomposing isotope patterns for metabolite identification†
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High-Throughput Miniaturized 16S rRNA Amplicon Library Preparation Reduces Costs while Preserving Microbiome Integrity
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Ion identity molecular networking for mass spectrometry-based metabolomics in the GNPS environment
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Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
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Optimizing sequencing protocols for leaderboard metagenomics by combining long and short reads
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Qiita: rapid, web-enabled microbiome meta-analysis
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Global patterns in belowground communities
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