The microbiologist's guide to metaproteomics

Van Den Bossche, Tim; Armengaud, Jean; Benndorf, Dirk; Blakeley‐Ruiz, Jose Alfredo; Brauer, Madita; Cheng, Kai; Creskey, Marybeth; Figeys, Daniel; Grenga, Lucia; Griffin, Timothy J.; Henry, Céline; Hettich, Robert L.; Holstein, Tanja; Jagtap, Pratik D.; Jehmlich, Nico; Kim, Jonghyun; Kleiner, Manuel; Kunath, Benoit J.; Malliet, Xuxa; Martens, Lennart; Mehta, Subina; Mesuere, Bart; Ning, Zhibin; Tanca, Alessandro; Uzzau, Sergio; Verschaffelt, Pieter; Wang, Jing; Wilmes, Paul; Zhang, Xu; Zhang, Xin; Li, Leyuan

doi:10.1002/imt2.70031

The microbiologist's guide to metaproteomics

Journal Article · Tue May 06 00:00:00 EDT 2025 · iMeta

DOI:https://doi.org/10.1002/imt2.70031· OSTI ID:2586845

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Ghent Univ. (Belgium)
Univ. Paris-Saclay (France)
Anhalt Univ. of Applied Sciences, Bernberg (Germany); Max Planck Institute for Dynamics of Complex Technical Systems (Germany); Otto von Guericke University (Germany)
North Carolina State University, Raleigh, NC (United States)
Univ. of Luxembourg, Esch-sur-Alzette, (Luxembourg)
Univ. of Ottawa, ON (Canada)
Health Canada, Ottawa, ON (Canada)
Univ. of Ottawa, ON (Canada); Quadram Institute Bioscience (United Kingdom); Univ. of East Anglia, Norwich (United Kingdom)
Univ. of Minnesota, Minneapolis, MN (United States)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Ghent Univ. (Belgium); Robert‐Koch‐Institut (Germany)
Helmholtz Centre for Environmental Research (UFZ) (Germany)
North Carolina State University, Raleigh, NC (United States); Univ. of Luxembourg, Esch-sur-Alzette, (Luxembourg)
Ghent Univ. (Belgium); University of Strasbourg (France)
Univ. of Sassari (Italy)
Beijing Institute of Lifeomics (China)

Metaproteomics is an emerging approach for studying microbiomes, offering the ability to characterize proteins that underpin microbial functionality within diverse ecosystems. As the primary catalytic and structural components of microbiomes, proteins provide unique insights into the active processes and ecological roles of microbial communities. By integrating metaproteomics with other omics disciplines, researchers can gain a comprehensive understanding of microbial ecology, interactions, and functional dynamics. This review, developed by the Metaproteomics Initiative (www.metaproteomics.org), serves as a practical guide for both microbiome and proteomics researchers, presenting key principles, state-of-the-art methodologies, and analytical workflows essential to metaproteomics. Topics covered include experimental design, sample preparation, mass spectrometry techniques, data analysis strategies, and statistical approaches.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2586845

Journal Information:: iMeta, Journal Name: iMeta Journal Issue: 3 Vol. 4; ISSN 2770-5986; ISSN 2770-596X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Bioaerosols in swine confinement buildings: A metaproteomic view Meyer, Susann; Hüttig, Nicole; Zenk, Marianne Environmental Microbiology Reports, Vol. 15, Issue 6 https://doi.org/10.1111/1758-2229.13208	journal	November 2023
Assessing the impact of interfering organic matter on soil metaproteomic workflow Waibel, Matthias; McDonnell, Kevin; Tuohy, Maria European Journal of Soil Science, Vol. 74, Issue 3 https://doi.org/10.1111/ejss.13392	journal	May 2023
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Illuminating Key Microbial Players and Metabolic Processes Involved in the Remineralization of Particulate Organic Carbon in the Ocean’s Twilight Zone by Metaproteomics Kong, Ling-Fen; He, Yan-Bin; Xie, Zhang-Xian Applied and Environmental Microbiology, Vol. 87, Issue 20 https://doi.org/10.1128/AEM.00986-21	journal	September 2021
Evaluation of RNA later as a Field-Compatible Preservation Method for Metaproteomic Analyses of Bacterium-Animal Symbioses Jensen, Marlene; Wippler, Juliane; Kleiner, Manuel Microbiology Spectrum, Vol. 9, Issue 2 https://doi.org/10.1128/Spectrum.01429-21	journal	October 2021
Evaluation of Sample Preservation and Storage Methods for Metaproteomics Analysis of Intestinal Microbiomes Mordant, Angie; Kleiner, Manuel Microbiology Spectrum, Vol. 9, Issue 3 https://doi.org/10.1128/Spectrum.01877-21	journal	December 2021
Posttranslational modifications: an emerging functional layer of diet-host-microbe interactions Duchovni, Lirit; Shmunis, Genrieta; Lobel, Lior mBio, Vol. 15, Issue 10 https://doi.org/10.1128/mbio.02387-24	journal	October 2024
A novel clinical metaproteomics workflow enables bioinformatic analysis of host-microbe dynamics in disease Do, Katherine; Mehta, Subina; Wagner, Reid mSphere, Vol. 9, Issue 6 https://doi.org/10.1128/msphere.00793-23	journal	June 2024
Metaproteomics: Much More than Measuring Gene Expression in Microbial Communities Kleiner, Manuel mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/msystems.00115-19	journal	May 2019
High-Throughput Stool Metaproteomics: Method and Application to Human Specimens Gonzalez, Carlos G.; Wastyk, Hannah C.; Topf, Madeline mSystems, Vol. 5, Issue 3 https://doi.org/10.1128/msystems.00200-20	journal	June 2020
MetaProClust-MS1: an MS1 Profiling Approach for Large-Scale Microbiome Screening Simopoulos, Caitlin M. A.; Ning, Zhibin; Li, Leyuan mSystems, Vol. 7, Issue 4 https://doi.org/10.1128/msystems.00381-22	journal	August 2022
Benchmarking low- and high-throughput protein cleanup and digestion methods for human fecal metaproteomics Tanca, Alessandro; Deledda, Maria Antonietta; De Diego, Laura mSystems, Vol. 9, Issue 7 https://doi.org/10.1128/msystems.00661-24	journal	July 2024
Association betweenBrachyspiraand irritable bowel syndrome with diarrhoea Jabbar, Karolina S.; Dolan, Brendan; Eklund, Lisbeth Gut, Vol. 70, Issue 6 https://doi.org/10.1136/gutjnl-2020-321466	journal	November 2020
Computational Methods for Understanding Mass Spectrometry–Based Shotgun Proteomics Data Sinitcyn, Pavel; Rudolph, Jan Daniel; Cox, Jürgen Annual Review of Biomedical Data Science, Vol. 1, Issue 1 https://doi.org/10.1146/annurev-biodatasci-080917-013516	journal	July 2018
Activity-Based Protein Profiling: From Enzyme Chemistry to Proteomic Chemistry Cravatt, Benjamin F.; Wright, Aaron T.; Kozarich, John W. Annual Review of Biochemistry, Vol. 77, Issue 1 https://doi.org/10.1146/annurev.biochem.75.101304.124125	journal	June 2008
IMP: a pipeline for reproducible reference-independent integrated metagenomic and metatranscriptomic analyses Narayanasamy, Shaman; Jarosz, Yohan; Muller, Emilie E. L. Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1116-8	journal	December 2016
Robust taxonomic classification of uncharted microbial sequences and bins with CAT and BAT von Meijenfeldt, F. A. Bastiaan; Arkhipova, Ksenia; Cambuy, Diego D. Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1817-x	journal	October 2019
Improved metagenomic analysis with Kraken 2 Wood, Derrick E.; Lu, Jennifer; Langmead, Ben Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1891-0	journal	November 2019
A straightforward and efficient analytical pipeline for metaproteome characterization Tanca, Alessandro; Palomba, Antonio; Pisanu, Salvatore Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/s40168-014-0049-2	journal	December 2014
MetaPro-IQ: a universal metaproteomic approach to studying human and mouse gut microbiota Zhang, Xu; Ning, Zhibin; Mayne, Janice Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0176-z	journal	June 2016
Post-translational modifications are enriched within protein functional groups important to bacterial adaptation within a deep-sea hydrothermal vent environment Zhang, Weipeng; Sun, Jin; Cao, Huiluo Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0194-x	journal	September 2016
The impact of sequence database choice on metaproteomic results in gut microbiota studies Tanca, Alessandro; Palomba, Antonio; Fraumene, Cristina Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0196-8	journal	September 2016
Genome-resolved metaproteomic characterization of preterm infant gut microbiota development reveals species-specific metabolic shifts and variabilities during early life Xiong, Weili; Brown, Christopher T.; Morowitz, Michael J. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0290-6	journal	July 2017
MetaLab: an automated pipeline for metaproteomic data analysis Cheng, Kai; Ning, Zhibin; Zhang, Xu Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0375-2	journal	December 2017
Metaproteomics reveals persistent and phylum-redundant metabolic functional stability in adult human gut microbiomes of Crohn’s remission patients despite temporal variations in microbial taxa, genomes, and proteomes Blakeley-Ruiz, J. Alfredo; Erickson, Alison R.; Cantarel, Brandi L. Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0631-8	journal	February 2019
The neovaginal microbiome of transgender women post-gender reassignment surgery Birse, Kenzie D.; Kratzer, Kateryna; Zuend, Christina Farr Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00804-1	journal	May 2020
RapidAIM: a culture- and metaproteomics-based Rapid Assay of Individual Microbiome responses to drugs Li, Leyuan; Ning, Zhibin; Zhang, Xu Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00806-z	journal	March 2020
Microbiome definition re-visited: old concepts and new challenges Berg, Gabriele; Rybakova, Daria; Fischer, Doreen Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00875-0	journal	June 2020
An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants Xie, Fei; Jin, Wei; Si, Huazhe Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-021-01078-x	journal	June 2021
The Metaproteomics Initiative: a coordinated approach for propelling the functional characterization of microbiomes Van Den Bossche, Tim; Arntzen, Magnus Ø.; Becher, Dörte Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-021-01176-w	journal	December 2021
Lactic acid from vaginal microbiota enhances cervicovaginal epithelial barrier integrity by promoting tight junction protein expression Delgado-Diaz, David Jose; Jesaveluk, Brianna; Hayward, Joshua A. Microbiome, Vol. 10, Issue 1 https://doi.org/10.1186/s40168-022-01337-5	journal	August 2022
Nanopore long-read-only metagenomics enables complete and high-quality genome reconstruction from mock and complex metagenomes Liu, Lei; Yang, Yu; Deng, Yu Microbiome, Vol. 10, Issue 1 https://doi.org/10.1186/s40168-022-01415-8	journal	December 2022
Alterations of oral microbiota and impact on the gut microbiome in type 1 diabetes mellitus revealed by integrated multi-omic analyses Kunath, B. J.; Hickl, O.; Queirós, P. Microbiome, Vol. 10, Issue 1 https://doi.org/10.1186/s40168-022-01435-4	journal	December 2022
Ultra-sensitive isotope probing to quantify activity and substrate assimilation in microbiomes Kleiner, Manuel; Kouris, Angela; Violette, Marlene Microbiome, Vol. 11, Issue 1 https://doi.org/10.1186/s40168-022-01454-1	journal	February 2023
metaSpectraST: an unsupervised and database-independent analysis workflow for metaproteomic MS/MS data using spectrum clustering Hao, Chunlin; Elias, Joshua E.; Lee, Patrick K. H. Microbiome, Vol. 11, Issue 1 https://doi.org/10.1186/s40168-023-01602-1	journal	August 2023
In-depth metaproteomics analysis of tongue coating for gastric cancer: a multicenter diagnostic research study Chen, Jiahui; Sun, Yingying; Li, Jie Microbiome, Vol. 12, Issue 1 https://doi.org/10.1186/s40168-023-01730-8	journal	January 2024
Novel functional insights into the microbiome inhabiting marine plastic debris: critical considerations to counteract the challenges of thin biofilms using multi-omics and comparative metaproteomics Messer, Lauren F.; Lee, Charlotte E.; Wattiez, Ruddy Microbiome, Vol. 12, Issue 1 https://doi.org/10.1186/s40168-024-01751-x	journal	February 2024
The astounding exhaustiveness and speed of the Astral mass analyzer for highly complex samples is a quantum leap in the functional analysis of microbiomes Dumas, Thibaut; Martinez Pinna, Roxana; Lozano, Clément Microbiome, Vol. 12, Issue 1 https://doi.org/10.1186/s40168-024-01766-4	journal	March 2024
Salivary proteomics and metaproteomics identifies distinct molecular and taxonomic signatures of type-2 diabetes Samodova, Diana; Stankevic, Evelina; Søndergaard, Mathilde Sonne Microbiome, Vol. 13, Issue 1 https://doi.org/10.1186/s40168-024-01997-5	journal	January 2025
PhyloFunc: phylogeny-informed functional distance as a new ecological metric for metaproteomic data analysis Wang, Luman; Simopoulos, Caitlin M. A.; Serrana, Joeselle M. Microbiome, Vol. 13, Issue 1 https://doi.org/10.1186/s40168-024-02015-4	journal	February 2025
Integrative meta-omics in Galaxy and beyond Schiml, Valerie C.; Delogu, Francesco; Kumar, Praveen Environmental Microbiome, Vol. 18, Issue 1 https://doi.org/10.1186/s40793-023-00514-9	journal	July 2023
Public human microbiome data are dominated by highly developed countries Abdill, Richard J.; Adamowicz, Elizabeth M.; Blekhman, Ran PLOS Biology, Vol. 20, Issue 2 https://doi.org/10.1371/journal.pbio.3001536	journal	February 2022
Comprehensive mouse microbiota genome catalog reveals major difference to its human counterpart Kieser, Silas; Zdobnov, Evgeny M.; Trajkovski, Mirko PLOS Computational Biology, Vol. 18, Issue 3 https://doi.org/10.1371/journal.pcbi.1009947	journal	March 2022
Galaxy Training: A powerful framework for teaching! Hiltemann, Saskia; Rasche, Helena; Gladman, Simon PLOS Computational Biology, Vol. 19, Issue 1 https://doi.org/10.1371/journal.pcbi.1010752	journal	January 2023
Modified TCA/acetone precipitation of plant proteins for proteomic analysis Niu, Liangjie; Zhang, Hang; Wu, Zhaokun PLOS ONE, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pone.0202238	journal	December 2018
Survey of metaproteomics software tools for functional microbiome analysis Sajulga, Ray; Easterly, Caleb; Riffle, Michael PLOS ONE, Vol. 15, Issue 11 https://doi.org/10.1371/journal.pone.0241503	journal	November 2020
Five key aspects of metaproteomics as a tool to understand functional interactions in host-associated microbiomes Salvato, Fernanda; Hettich, Robert L.; Kleiner, Manuel PLOS Pathogens, Vol. 17, Issue 2 https://doi.org/10.1371/journal.ppat.1009245	journal	February 2021
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Exoproteomics: exploring the world around biological systems Armengaud, Jean; Christie-Oleza, Joseph A.; Clair, Gérémy Expert Review of Proteomics, Vol. 9, Issue 5 https://doi.org/10.1586/epr.12.52	journal	October 2012
RapidAIM 2.0: a high-throughput assay to study functional response of human gut microbiome to xenobiotics Li, Leyuan; Mayne, Janice; Beltran, Adrian Microbiome Research Reports, Vol. 3, Issue 2 https://doi.org/10.20517/mrr.2023.57	journal	April 2024
Assessing fecal metaproteomics workflow and small protein recovery using DDA and DIA PASEF mass spectrometry Wang, Angela; Fekete, Emily E. F.; Creskey, Marybeth Microbiome Research Reports, Vol. 3, Issue 3 https://doi.org/10.20517/mrr.2024.21	journal	July 2024
An Innovative Protocol for Metaproteomic Analyses of Microbial Pathogens in Cystic Fibrosis Sputum Graf, Alexander C.; Striesow, Johanna; Pané-Farré, Jan Frontiers in Cellular and Infection Microbiology, Vol. 11 https://doi.org/10.3389/fcimb.2021.724569	journal	August 2021
Examination of Microbial Proteome Preservation Techniques Applicable to Autonomous Environmental Sample Collection Saito, Mak A.; Bulygin, Vladimir V.; Moran, Dawn M. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00215	journal	January 2011
Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant Brooks, Brandon; Mueller, Ryan S.; Young, Jacque C. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00654	journal	July 2015
Metaproteogenomics Reveals Taxonomic and Functional Changes between Cecal and Fecal Microbiota in Mouse Tanca, Alessandro; Manghina, Valeria; Fraumene, Cristina Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00391	journal	March 2017
A Structural and Functional Elucidation of the Rumen Microbiome Influenced by Various Diets and Microenvironments Deusch, Simon; Camarinha-Silva, Amélia; Conrad, Jürgen Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01605	journal	August 2017
More Is Not Always Better: Evaluation of 1D and 2D-LC-MS/MS Methods for Metaproteomics Hinzke, Tjorven; Kouris, Angela; Hughes, Rebecca-Ayme Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00238	journal	February 2019
A Robust and Universal Metaproteomics Workflow for Research Studies and Routine Diagnostics Within 24 h Using Phenol Extraction, FASP Digest, and the MetaProteomeAnalyzer Heyer, Robert; Schallert, Kay; Büdel, Anja Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01883	journal	August 2019
Genome-Resolved Proteomic Stable Isotope Probing of Soil Microbial Communities Using 13CO2 and 13C-Methanol Li, Zhou; Yao, Qiuming; Guo, Xuan Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02706	journal	December 2019
Quantitative metaproteomics reveals composition and metabolism characteristics of microbial communities in Chinese liquor fermentation starters Zhao, Jinzhi; Yang, Yi; Chen, Liangqiang Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.1098268	journal	January 2023
Comprehensive Metabolic and Taxonomic Reconstruction of an Ancient Microbial Mat From the McMurdo Ice Shelf (Antarctica) by Integrating Genetic, Metaproteomic and Lipid Biomarker Analyses Lezcano, María Ángeles; Sánchez-García, Laura; Quesada, Antonio Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.799360	journal	April 2022
Metaproteomic Profile of the Colonic Luminal Microbiota From Patients With Colon Cancer Tanca, Alessandro; Abbondio, Marcello; Fiorito, Giovanni Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.869523	journal	April 2022
Taxonomical composition and functional analysis of biofilms sampled from a nuclear storage pool Pible, Olivier; Petit, Pauline; Steinmetz, Gérard Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1148976	journal	April 2023
Increasing taxonomic and functional characterization of host-microbiome interactions by DIA-PASEF metaproteomics Gómez-Varela, David; Xian, Feng; Grundtner, Sabrina Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1258703	journal	October 2023
Metaproteomics profiling of the microbial communities in fermentation starters (Daqu) during multi-round production of Chinese liquor Zhao, Jinzhi; Yang, Yi; Teng, Mengjing Frontiers in Nutrition, Vol. 10 https://doi.org/10.3389/fnut.2023.1139836	journal	June 2023
Quality Control—A Stepchild in Quantitative Proteomics: A Case Study for the Human CSF Proteome Rozanova, Svitlana; Uszkoreit, Julian; Schork, Karin Biomolecules, Vol. 13, Issue 3 https://doi.org/10.3390/biom13030491	journal	March 2023
Modern Metaproteomics: A Unique Tool to Characterize the Active Microbiome in Health and Diseases, and Pave the Road towards New Biomarkers—Example of Crohn’s Disease and Ulcerative Colitis Flare-Ups Henry, Céline; Bassignani, Ariane; Berland, Magali Cells, Vol. 11, Issue 8 https://doi.org/10.3390/cells11081340	journal	April 2022
The Farmed Atlantic Salmon (Salmo salar) Skin–Mucus Proteome and Its Nutrient Potential for the Resident Bacterial Community Minniti, Giusi; Rød Sandve, Simen; Padra, János Tamás Genes, Vol. 10, Issue 7 https://doi.org/10.3390/genes10070515	journal	July 2019
The Simplified Human Intestinal Microbiota (SIHUMIx) Shows High Structural and Functional Resistance against Changing Transit Times in In Vitro Bioreactors Schäpe, Stephanie Serena; Krause, Jannike Lea; Engelmann, Beatrice Microorganisms, Vol. 7, Issue 12 https://doi.org/10.3390/microorganisms7120641	journal	December 2019
Disseminating Metaproteomic Informatics Capabilities and Knowledge Using the Galaxy-P Framework Blank, Clemens; Easterly, Caleb; Gruening, Bjoern Proteomes, Vol. 6, Issue 1 https://doi.org/10.3390/proteomes6010007	journal	January 2018
Bacterial symbiont subpopulations have different roles in a deep-sea symbiosis Hinzke, Tjorven; Kleiner, Manuel; Meister, Mareike eLife, Vol. 10 https://doi.org/10.7554/eLife.58371	journal	January 2021
A combined test for feature selection on sparse metaproteomics data—an alternative to missing value imputation Plancade, Sandra; Berland, Magali; Blein-Nicolas, Mélisande PeerJ, Vol. 10 https://doi.org/10.7717/peerj.13525	journal	June 2022

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