Microbial community proteomics for characterizing the range of metabolic functions and activities of human gut microbiota

Xiong, Weili; Abraham, Paul E.; Li, Zhou; Pan, Chongle

doi:10.1002/pmic.201400571

Microbial community proteomics for characterizing the range of metabolic functions and activities of human gut microbiota

Journal Article · Fri Apr 24 00:00:00 EDT 2015 · Proteomics (Online)

DOI:https://doi.org/10.1002/pmic.201400571· OSTI ID:1237607

Xiong, Weili ^[1]; Abraham, Paul E. ^[2]; Li, Zhou ^[2]; Pan, Chongle ^[2]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

We found that the human gastrointestinal (GI) tract is a complex, dynamic ecosystem that consists of a carefully tuned balance of human host and microbiota membership. The microbiome component is not insignificant, but rather provides important functions that are absolutely critical to many aspects of human health, including nutrient transformation and absorption, drug metabolism, pathogen defense, and immune system development. Microbial community proteomics (sometimes referred to as metaproteomics) provides a powerful approach to measure the range and details of human gut microbiota functions and metabolic activities, revealing information about microbiome development and stability especially with regard to human health vs. disease states. In most cases, both microbial and human proteins are extracted from fecal samples and then measured by the high performance MS-based proteomics technology. We review the field of human gut microbiome community proteomics, with a focus on the experimental and informatics considerations involved in characterizing systems that range from low complexity defined model gut microbiota in gnotobiotic mice, to the simple gut microbiota in the GI tract of newborn infants, and finally to the complex gut microbiota in adults. Moreover, the current state-of-the-art in experimental and bioinformatics capabilities for community proteomics enable a detailed measurement of the gut microbiota, yielding valuable insights into the broad functional profiles of even complex microbiota. Future developments are likely to expand into improved analysis throughput and coverage depth, as well as post-translational modification characterizations.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE; National Institutes of Health (NIH)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1237607

Journal Information:: Proteomics (Online), Journal Name: Proteomics (Online) Journal Issue: 20 Vol. 15; ISSN 1615-9861

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (77)

Probability-based protein identification by searching sequence databases using mass spectrometry data Perkins, David N.; Pappin, Darryl J. C.; Creasy, David M. Electrophoresis, Vol. 20, Issue 18 https://doi.org/10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2	journal	December 1999
Host–microbe relationships in inflammatory bowel disease detected by bacterial and metaproteomic analysis of the mucosal–luminal interface Presley, Laura L.; Ye, Jingxiao; Li, Xiaoxiao Inflammatory Bowel Diseases, Vol. 18, Issue 3 https://doi.org/10.1002/ibd.21793	journal	March 2012
Mass spectrometry-based metabolomics Dettmer, Katja; Aronov, Pavel A.; Hammock, Bruce D. Mass Spectrometry Reviews, Vol. 26, Issue 1 https://doi.org/10.1002/mas.20108	journal	January 2006
Protein-based stable isotope probing (protein-SIP) in functional metaproteomics Seifert, Jana; Taubert, Martin; Jehmlich, Nico Mass Spectrometry Reviews, Vol. 31, Issue 6 https://doi.org/10.1002/mas.21346	journal	March 2012
A computational method for assessing peptide- identification reliability in tandem mass spectrometry analysis with SEQUEST Razumovskaya, Jane; Olman, Victor; Xu, Dong PROTEOMICS, Vol. 4, Issue 4 https://doi.org/10.1002/pmic.200300656	journal	April 2004
Proteomic investigation of the adaptation ofLactococcus lactis to the mouse digestive tract Roy, Karine; Meyrand, Mickaël; Corthier, Gérard PROTEOMICS, Vol. 8, Issue 8 https://doi.org/10.1002/pmic.200700698	journal	April 2008
Bioinformatic progress and applications in metaproteogenomics for bridging the gap between genomic sequences and metabolic functions in microbial communities Seifert, Jana; Herbst, Florian-Alexander; Halkjaer Nielsen, Per PROTEOMICS, Vol. 13, Issue 18-19 https://doi.org/10.1002/pmic.201200566	journal	August 2013
Metaproteomics to unravel major microbial players in leaf litter and soil environments: Challenges and perspectives Becher, Dörte; Bernhardt, Jörg; Fuchs, Stephan PROTEOMICS, Vol. 13, Issue 18-19 https://doi.org/10.1002/pmic.201300095	journal	October 2013
Quantitative proteomics in the field of microbiology Otto, Andreas; Becher, Dörte; Schmidt, Frank PROTEOMICS, Vol. 14, Issue 4-5 https://doi.org/10.1002/pmic.201300403	journal	March 2014
Metaproteomics reveals functional shifts in microbial and human proteins during a preterm infant gut colonization case Young, Jacque C.; Pan, Chongle; Adams, Rachel M. PROTEOMICS, Vol. 15, Issue 20 https://doi.org/10.1002/pmic.201400563	journal	July 2015
Quantitative Metaproteomics: Functional Insights into Microbial Communities Pan, Chongle; Banfield, Jillian F. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-712-9_18	book	January 2014
An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database Eng, Jimmy K.; McCormack, Ashley L.; Yates, John R. Journal of the American Society for Mass Spectrometry, Vol. 5, Issue 11 https://doi.org/10.1016/1044-0305(94)80016-2	journal	November 1994
SILAC Mouse for Quantitative Proteomics Uncovers Kindlin-3 as an Essential Factor for Red Blood Cell Function Krüger, Marcus; Moser, Markus; Ussar, Siegfried Cell, Vol. 134, Issue 2 https://doi.org/10.1016/j.cell.2008.05.033	journal	July 2008
The Impact of the Gut Microbiota on Human Health: An Integrative View Clemente, Jose C.; Ursell, Luke K.; Parfrey, Laura Wegener Cell, Vol. 148, Issue 6 https://doi.org/10.1016/j.cell.2012.01.035	journal	March 2012
Correlation of mRNA and protein in complex biological samples Maier, Tobias; Güell, Marc; Serrano, Luis FEBS Letters, Vol. 583, Issue 24 https://doi.org/10.1016/j.febslet.2009.10.036	journal	October 2009
Metaproteomics of our microbiome — Developing insight in function and activity in man and model systems Kolmeder, Carolin A.; de Vos, Willem M. Journal of Proteomics, Vol. 97 https://doi.org/10.1016/j.jprot.2013.05.018	journal	January 2014
Microbial metaproteomics: identifying the repertoire of proteins that microorganisms use to compete and cooperate in complex environmental communities Hettich, Robert L.; Sharma, Ritin; Chourey, Karuna Current Opinion in Microbiology, Vol. 15, Issue 3 https://doi.org/10.1016/j.mib.2012.04.008	journal	June 2012
Development of intestinal microbiota in infants and its impact on health Matamoros, Sebastien; Gras-Leguen, Christele; Le Vacon, Françoise Trends in Microbiology, Vol. 21, Issue 4 https://doi.org/10.1016/j.tim.2012.12.001	journal	April 2013
DBDigger: Reorganized Proteomic Database Identification That Improves Flexibility and Speed Tabb, David L.; Narasimhan, Chandrasegaran; Strader, Michael Brad Analytical Chemistry, Vol. 77, Issue 8 https://doi.org/10.1021/ac0487000	journal	April 2005
Metaproteomics : Harnessing the Power of High Performance Mass Spectrometry to Identify the Suite of Proteins That Control Metabolic Activities in Microbial Communities Hettich, Robert L.; Pan, Chongle; Chourey, Karuna Analytical Chemistry, Vol. 85, Issue 9 https://doi.org/10.1021/ac303053e	journal	March 2013
Multidimensional LC Separations in Shotgun Proteomics Motoyama, Akira; Yates, John R. Analytical Chemistry, Vol. 80, Issue 19 https://doi.org/10.1021/ac8013669	journal	October 2008
Stable-Isotope Probing Reveals That Hydrogen Isotope Fractionation in Proteins and Lipids in a Microbial Community Are Different and Species-Specific Fischer, Curt R.; Bowen, Benjamin P.; Pan, Chongle ACS Chemical Biology, Vol. 8, Issue 8 https://doi.org/10.1021/cb400210q	journal	June 2013
Open Mass Spectrometry Search Algorithm Geer, Lewis Y.; Markey, Sanford P.; Kowalak, Jeffrey A. Journal of Proteome Research, Vol. 3, Issue 5 https://doi.org/10.1021/pr0499491	journal	October 2004
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C. Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr0604054	journal	February 2007
Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics Chourey, Karuna; Jansson, Janet; VerBerkmoes, Nathan Journal of Proteome Research, Vol. 9, Issue 12 https://doi.org/10.1021/pr100787q	journal	December 2010
Systematic Comparison of Label-Free, Metabolic Labeling, and Isobaric Chemical Labeling for Quantitative Proteomics on LTQ Orbitrap Velos Li, Zhou; Adams, Rachel M.; Chourey, Karuna Journal of Proteome Research, Vol. 11, Issue 3 https://doi.org/10.1021/pr200748h	journal	January 2012
Defining the Boundaries and Characterizing the Landscape of Functional Genome Expression in Vascular Tissues of Populus using Shotgun Proteomics Abraham, Paul; Adams, Rachel; Giannone, Richard J. Journal of Proteome Research, Vol. 11, Issue 1 https://doi.org/10.1021/pr200851y	journal	November 2011
Coupling a Detergent Lysis/Cleanup Methodology with Intact Protein Fractionation for Enhanced Proteome Characterization Sharma, Ritin; Dill, Brian D.; Chourey, Karuna Journal of Proteome Research, Vol. 11, Issue 12 https://doi.org/10.1021/pr300709k	journal	October 2012
Human gut microbes associated with obesity Ley, Ruth E.; Turnbaugh, Peter J.; Klein, Samuel Nature, Vol. 444, Issue 7122 https://doi.org/10.1038/4441022a	journal	December 2006
Large-scale analysis of the yeast proteome by multidimensional protein identification technology Washburn, Michael P.; Wolters, Dirk; Yates, John R. Nature Biotechnology, Vol. 19, Issue 3 https://doi.org/10.1038/85686	journal	March 2001
Shotgun metaproteomics of the human distal gut microbiota Verberkmoes, Nathan C.; Russell, Alison L.; Shah, Manesh The ISME Journal, Vol. 3, Issue 2 https://doi.org/10.1038/ismej.2008.108	journal	October 2008
Insights from quantitative metaproteomics and protein-stable isotope probing into microbial ecology von Bergen, Martin; Jehmlich, Nico; Taubert, Martin The ISME Journal, Vol. 7, Issue 10 https://doi.org/10.1038/ismej.2013.78	journal	May 2013
Nutrients drive transcriptional changes that maintain metabolic homeostasis but alter genome architecture in Microcystis Steffen, Morgan M.; Dearth, Stephen P.; Dill, Brian D. The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.78	journal	May 2014
The International HapMap Project Consortium, International HapMap Nature, Vol. 426, Issue 6968, p. 789-796 https://doi.org/10.1038/nature02168	journal	January 2003
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination Berer, Kerstin; Mues, Marsilius; Koutrolos, Michail Nature, Vol. 479, Issue 7374 https://doi.org/10.1038/nature10554	journal	October 2011
Diversity, stability and resilience of the human gut microbiota Lozupone, Catherine A.; Stombaugh, Jesse I.; Gordon, Jeffrey I. Nature, Vol. 489, Issue 7415 https://doi.org/10.1038/nature11550	journal	September 2012
The African Genome Variation Project shapes medical genetics in Africa Gurdasani, Deepti; Carstensen, Tommy; Tekola-Ayele, Fasil Nature, Vol. 517, Issue 7534 https://doi.org/10.1038/nature13997	journal	December 2014
Diverse and divergent protein post-translational modifications in two growth stages of a natural microbial community Li, Zhou; Wang, Yingfeng; Yao, Qiuming Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5405	journal	July 2014
Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Elias, Joshua E.; Gygi, Steven P. Nature Methods, Vol. 4, Issue 3 https://doi.org/10.1038/nmeth1019	journal	February 2007
Large-scale database searching using tandem mass spectra: Looking up the answer in the back of the book Sadygov, Rovshan G.; Cociorva, Daniel; Yates, John R. Nature Methods, Vol. 1, Issue 3 https://doi.org/10.1038/nmeth725	journal	November 2004
Insights into the regulation of protein abundance from proteomic and transcriptomic analyses Vogel, Christine; Marcotte, Edward M. Nature Reviews Genetics, Vol. 13, Issue 4 https://doi.org/10.1038/nrg3185	journal	March 2012
The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models Nell, Sandra; Suerbaum, Sebastian; Josenhans, Christine Nature Reviews Microbiology, Vol. 8, Issue 8 https://doi.org/10.1038/nrmicro2403	journal	July 2010
Searching for a needle in a stack of needles: challenges in metaproteomics data analysis Muth, Thilo; Benndorf, Dirk; Reichl, Udo Mol. BioSyst., Vol. 9, Issue 4 https://doi.org/10.1039/C2MB25415H	journal	January 2013
Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla Mahowald, M. A.; Rey, F. E.; Seedorf, H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 14 https://doi.org/10.1073/pnas.0901529106	journal	March 2009
Quantitative Tracking of Isotope Flows in Proteomes of Microbial Communities Pan, Chongle; Fischer, Curt R.; Hyatt, Doug Molecular & Cellular Proteomics, Vol. 10, Issue 4 https://doi.org/10.1074/mcp.M110.006049	journal	February 2011
Status of Large-scale Analysis of Post-translational Modifications by Mass Spectrometry Olsen, Jesper V.; Mann, Matthias Molecular & Cellular Proteomics, Vol. 12, Issue 12 https://doi.org/10.1074/mcp.O113.034181	journal	November 2013
Interpretation of Shotgun Proteomic Data: The Protein Inference Problem Nesvizhskii, Alexey I.; Aebersold, Ruedi Molecular & Cellular Proteomics, Vol. 4, Issue 10 https://doi.org/10.1074/mcp.R500012-MCP200	journal	July 2005
TANDEM: matching proteins with tandem mass spectra Craig, R.; Beavis, R. C. Bioinformatics, Vol. 20, Issue 9 https://doi.org/10.1093/bioinformatics/bth092	journal	February 2004
Exhaustive database searching for amino acid mutations in proteomes Hyatt, Doug; Pan, Chongle Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts274	journal	May 2012
Sipros/ProRata: a versatile informatics system for quantitative community proteomics Wang, Yingfeng; Ahn, Tae-Hyuk; Li, Zhou Bioinformatics, Vol. 29, Issue 16 https://doi.org/10.1093/bioinformatics/btt329	journal	June 2013
Omega: an Overlap-graph de novo Assembler for Metagenomics Haider, Bahlul; Ahn, Tae-Hyuk; Bushnell, Brian Bioinformatics, Vol. 30, Issue 19 https://doi.org/10.1093/bioinformatics/btu395	journal	June 2014
The COG database: a tool for genome-scale analysis of protein functions and evolution Tatusov, R. L. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.33	journal	January 2000
¹⁵ N- and ² H proteomic stable isotope probing links nitrogen flow to archaeal heterotrophic activity : Tracking nitrogen flow with proteomic-SIP Justice, Nicholas B.; Li, Zhou; Wang, Yingfeng Environmental Microbiology, Vol. 16, Issue 10 https://doi.org/10.1111/1462-2920.12488	journal	May 2014
Adaptation of protein expression by Escherichia coli in the gastrointestinal tract of gnotobiotic mice Alpert, Carl; Scheel, Jacqueline; Engst, Wolfram Environmental Microbiology, Vol. 11, Issue 4 https://doi.org/10.1111/j.1462-2920.2008.01798.x	journal	April 2009
Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure: Metaproteomic insights associated to human obesity Ferrer, Manuel; Ruiz, Alicia; Lanza, Francesca Environmental Microbiology, Vol. 15, Issue 1 https://doi.org/10.1111/j.1462-2920.2012.02845.x	journal	August 2012
Exploring mixed microbial community functioning: recent advances in metaproteomics Siggins, Alma; Gunnigle, Eoin; Abram, Florence FEMS Microbiology Ecology, Vol. 80, Issue 2 https://doi.org/10.1111/j.1574-6941.2011.01284.x	journal	January 2012
Community Proteomics of a Natural Microbial Biofilm Ram, R. J. Science, Vol. 308, Issue 5730 https://doi.org/10.1126/science. 1109070	journal	June 2005
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages Ottesen, E. A.; Young, C. R.; Gifford, S. M. Science, Vol. 345, Issue 6193 https://doi.org/10.1126/science.1252476	journal	July 2014
The Application of the Nitrogen Isotope N ¹⁵ for the Study of Protein Metabolism Schoenheimer, Rudolf; Rittenberg, D.; Foster, G. L. Science, Vol. 88, Issue 2295 https://doi.org/10.1126/science.88.2295.599	journal	December 1938
Metaproteomics Approach To Study the Functionality of the Microbiota in the Human Infant Gastrointestinal Tract Klaassens, E. S.; de Vos, W. M.; Vaughan, E. E. Applied and Environmental Microbiology, Vol. 73, Issue 4 https://doi.org/10.1128/AEM.01921-06	journal	December 2006
Environmental Proteomics: a Paradigm Shift in Characterizing Microbial Activities at the Molecular Level Keller, M.; Hettich, R. Microbiology and Molecular Biology Reviews, Vol. 73, Issue 1 https://doi.org/10.1128/MMBR.00028-08	journal	March 2009
A comparison of cataloged variation between International HapMap Consortium and 1000 Genomes Project data Buchanan, Carrie C.; Torstenson, Eric S.; Bush, William S. Journal of the American Medical Informatics Association, Vol. 19, Issue 2 https://doi.org/10.1136/amiajnl-2011-000652	journal	March 2012
Bacterial protein signals are associated with Crohn’s disease Juste, Catherine; Kreil, David P.; Beauvallet, Christian Gut, Vol. 63, Issue 10 https://doi.org/10.1136/gutjnl-2012-303786	journal	January 2014
Combining gene prediction methods to improve metagenomic gene annotation Yok, Non G.; Rosen, Gail L. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-20	journal	January 2011
An iterative workflow for mining the human intestinal metaproteome Rooijers, Koos; Kolmeder, Carolin; Juste, Catherine BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-6	journal	January 2011
Development of the preterm infant gut microbiome: a research priority Groer, Maureen W.; Luciano, Angel A.; Dishaw, Larry J. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-38	journal	January 2014
Functional phylogenomics analysis of bacteria and archaea using consistent genome annotation with UniFam Chai, Juanjuan; Kora, Guruprasad; Ahn, Tae-Hyuk BMC Evolutionary Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12862-014-0207-y	journal	October 2014
Effects of Diet on Resource Utilization by a Model Human Gut Microbiota Containing Bacteroides cellulosilyticus WH2, a Symbiont with an Extensive Glycobiome McNulty, Nathan P.; Wu, Meng; Erickson, Alison R. PLoS Biology, Vol. 11, Issue 8 https://doi.org/10.1371/journal.pbio.1001637	journal	August 2013
A Metaproteomic Approach to Study Human-Microbial Ecosystems at the Mucosal Luminal Interface Li, Xiaoxiao; LeBlanc, James; Truong, Allison PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0026542	journal	November 2011
Strategies for Metagenomic-Guided Whole-Community Proteomics of Complex Microbial Environments Cantarel, Brandi L.; Erickson, Alison R.; VerBerkmoes, Nathan C. PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0027173	journal	November 2011
Comparative Metaproteomics and Diversity Analysis of Human Intestinal Microbiota Testifies for Its Temporal Stability and Expression of Core Functions Kolmeder, Carolin A.; de Been, Mark; Nikkilä, Janne PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0029913	journal	January 2012
Integrated Metagenomics/Metaproteomics Reveals Human Host-Microbiota Signatures of Crohn's Disease Erickson, Alison R.; Cantarel, Brandi L.; Lamendella, Regina PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0049138	journal	November 2012
Comparative Microbial Analysis of Paired Amniotic Fluid and Cord Blood from Pregnancies Complicated by Preterm Birth and Early-Onset Neonatal Sepsis Wang, Xiaowei; Buhimschi, Catalin S.; Temoin, Stephanie PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0056131	journal	February 2013
Meconium Microbiome Analysis Identifies Bacteria Correlated with Premature Birth Ardissone, Alexandria N.; de la Cruz, Diomel M.; Davis-Richardson, Austin G. PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0090784	journal	March 2014
Gut microbiota disturbance during antibiotic therapy Ferrer, Manuel; Martins dos Santos, Vitor AP; Ott, Stephan J. Gut Microbes, Vol. 5, Issue 1 https://doi.org/10.4161/gmic.27128	journal	December 2013

Cited By (15)

Gut microbiota functions: metabolism of nutrients and other food components Rowland, Ian; Gibson, Glenn; Heinken, Almut European Journal of Nutrition, Vol. 57, Issue 1 https://doi.org/10.1007/s00394-017-1445-8	journal	April 2017
Systems biology perspective for studying the gut microbiota in human physiology and liver diseases Altay, Ozlem; Nielsen, Jens; Uhlen, Mathias eBioMedicine, Vol. 49 https://doi.org/10.1016/j.ebiom.2019.09.057	journal	November 2019
Sipros Ensemble improves database searching and filtering for complex metaproteomics Guo, Xuan; Li, Zhou; Yao, Qiuming Bioinformatics, Vol. 34, Issue 5 https://doi.org/10.1093/bioinformatics/btx601	journal	September 2017
Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles Brown, Christopher T.; Xiong, Weili; Olm, Matthew R. mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mbio.00441-18	journal	April 2018
A comprehensive and scalable database search system for metaproteomics Chatterjee, Sandip; Stupp, Gregory S.; Park, Sung Kyu Robin BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2855-3	journal	August 2016
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
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
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
“Omic” investigations of protozoa and worms for a deeper understanding of the human gut “parasitome” Marzano, Valeria; Mancinelli, Livia; Bracaglia, Giorgia PLOS Neglected Tropical Diseases, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pntd.0005916	journal	November 2017
Metaproteomics as a Complementary Approach to Gut Microbiota in Health and Disease Petriz, Bernardo A.; Franco, Octávio L. Frontiers in Chemistry, Vol. 5 https://doi.org/10.3389/fchem.2017.00004	journal	January 2017
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
Association Between Gut Microbiota and CD4 Recovery in HIV-1 Infected Patients Lu, Wei; Feng, Yuqing; Jing, Fanhui Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01451	journal	July 2018
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
Microcins in Enterobacteriaceae: Peptide Antimicrobials in the Eco-Active Intestinal Chemosphere Baquero, Fernando; Lanza, Val F.; Baquero, Maria-Rosario Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02261	journal	October 2019
Metaproteomic and 16S rRNA Gene Sequencing Analysis of the Infant Fecal Microbiome Cortes, Laetitia; Wopereis, Harm; Tartiere, Aude International Journal of Molecular Sciences, Vol. 20, Issue 6 https://doi.org/10.3390/ijms20061430	journal	March 2019

Similar Records

Shotgun Metaproteomics of the Human Distal Gut Microbiota

Journal Article · Wed Dec 31 23:00:00 EST 2008 · Nature Methods · OSTI ID:958920

Shotgun metaproteomics of the human distal gut microbiota

Journal Article · Wed Oct 15 00:00:00 EDT 2008 · International Society for Microbial Ecology Journal · OSTI ID:943452

Development of an Enhanced Metaproteomic Approach for Deepening the Microbiome Characterization of the Human Infant Gut

Journal Article · Tue Oct 28 00:00:00 EDT 2014 · Journal of Proteome Research · OSTI ID:1185517

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Human gut microbiome
Metaproteomics
Shotgun proteomics
Systems biology

Microbial community proteomics for characterizing the range of metabolic functions and activities of human gut microbiota

Citation Formats

References (77)

Cited By (15)

Similar Records

Related Subjects