Skip to main content

Impact of Gut Microbiota on Host by Exploring Proteomics

  • Chapter
  • First Online:
Gut Microbiome and Its Impact on Health and Diseases

Abstract

Microbial colonization of intestine plays an important role in many aspects of human health. The growing availability of microbial genome sequences and advances in complementary transcriptomics and proteomics techniques are helping to better understand the link between the gut microbiome and human health. Proteomics combined with computational and bioinformatic tools and models are further aiding the progress in this field. However, many challenges still remain ahead to translate new knowledge gained from proteomics into disease diagnosis and treatment strategies. Future studies should focus on how to exploit these new technologies to advance our knowledge of gut microbiota in the context of human health and disease treatments. This book chapter discusses the application of proteomic techniques to explore gut microbial communities and future perspectives for advancing the field forward.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Altelaar, A. F., Munoz, J., & Heck, A. J. (2013). Next-generation proteomics: Towards an integrative view of proteome dynamics. Nature Reviews Genetics, 14(1), 35–48.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, N. L. (2018). Dynamics of clinically important proteins: Measuring turnover of drug targets and biomarkers. Clinical Chemistry, 64(2), 247–248.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, N. L., Ptolemy, A. S., & Rifai, N. (2013). The riddle of protein diagnostics: Future bleak or bright? Clinical Chemistry, 59(1), 194–197.

    Article  CAS  PubMed  Google Scholar 

  • Angel, T. E., Luft, B. J., Yang, X., Nicora, C. D., Camp, D. G., 2nd, Jacobs, J. M., & Smith, R. D. (2010). Proteome analysis of Borrelia burgdorferi response to environmental change. PLoS One, 5(11), e13800.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Angel, T. E., Aryal, U. K., Hengel, S. M., Baker, E. S., Kelly, R. T., Robinson, E. W., & Smith, R. D. (2012a). Mass spectrometry-based proteomics: Existing capabilities and future directions. Chemical Society Reviews, 41(10), 3912–3928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angel, T. E., Jacobs, J. M., Smith, R. P., Pasternack, M. S., Elias, S., Gritsenko, M. A., Shukla, A., Gilmore, E. C., McCarthy, C., Camp, D. G., 2nd, Smith, R. D., & Warren, H. S. (2012b). Cerebrospinal fluid proteome of patients with acute Lyme disease. Journal of Proteome Research, 11(10), 4814–4822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angel, T. E., Jacobs, J. M., Spudich, S. S., Gritsenko, M. A., Fuchs, D., Liegler, T., Zetterberg, H., Camp, D. G., 2nd, Price, R. W., & Smith, R. D. (2012c). The cerebrospinal fluid proteome in HIV infection: Change associated with disease severity. Clinical Proteomics, 9(1), 3.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aryal, U. K., & Ross, A. R. (2010). Enrichment and analysis of phosphopeptides under different experimental conditions using titanium dioxide affinity chromatography and mass spectrometry. Rapid Communications in Mass Spectrometry, 24(2), 219–231.

    Article  CAS  PubMed  Google Scholar 

  • Aryal, U. K., Olson, D. J., & Ross, A. R. (2008). Optimization of immobilized gallium (III) ion affinity chromatography for selective binding and recovery of phosphopeptides from protein digests. Journal of Biomolecular Techniques, 19(5), 296–310.

    PubMed  PubMed Central  Google Scholar 

  • Aryal, U. K., Stockel, J., Krovvidi, R. K., Gritsenko, M. A., Monroe, M. E., Moore, R. J., Koppenaal, D. W., Smith, R. D., Pakrasi, H. B., & Jacobs, J. M. (2011). Dynamic proteomic profiling of a unicellular cyanobacterium Cyanothece ATCC51142 across light-dark diurnal cycles. BMC Systems Biology, 5, 194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aryal, U. K., Stockel, J., Welsh, E. A., Gritsenko, M. A., Nicora, C. D., Koppenaal, D. W., Smith, R. D., Pakrasi, H. B., & Jacobs, J. M. (2012). Dynamic proteome analysis of Cyanothece sp. ATCC 51142 under constant light. Journal of Proteome Research, 11(2), 609–619.

    Article  CAS  PubMed  Google Scholar 

  • Aryal, U. K., Callister, S. J., Mishra, S., Zhang, X., Shutthanandan, J. I., Angel, T. E., Shukla, A. K., Monroe, M. E., Moore, R. J., Koppenaal, D. W., Smith, R. D., & Sherman, L. (2013). Proteome analyses of strains ATCC 51142 and PCC 7822 of the diazotrophic cyanobacterium Cyanothece sp. under culture conditions resulting in enhanced H(2) production. Applied and Environmental Microbiology, 79(4), 1070–1077.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aryal, U. K., Callister, S. J., McMahon, B. H., McCue, L. A., Brown, J., Stockel, J., Liberton, M., Mishra, S., Zhang, X., Nicora, C. D., Angel, T. E., Koppenaal, D. W., Smith, R. D., Pakrasi, H. B., & Sherman, L. A. (2014). Proteomic profiles of five strains of oxygenic photosynthetic cyanobacteria of the genus Cyanothece. Journal of Proteome Research, 13(7), 3262–3276.

    Article  CAS  PubMed  Google Scholar 

  • Aryal, U. K., McBride, Z., Chen, D., Xie, J., & Szymanski, D. B. (2017). Analysis of protein complexes in Arabidopsis leaves using size exclusion chromatography and label-free protein correlation profiling. Journal of Proteomics, 166, 8–18.

    Article  CAS  PubMed  Google Scholar 

  • Bache, N., Geyer, P. E., Bekker-Jensen, D. B., Hoerning, O., Falkenby, L., Treit, P. V., Doll, S., Paron, I., Muller, J. B., Meier, F., Olsen, J. V., Vorm, O., & Mann, M. (2018). A novel LC system embeds analytes in pre-formed gradients for rapid, ultra-robust proteomics. Molecular & Cellular Proteomics, 17(11), 2284–2296.

    Article  CAS  Google Scholar 

  • Bantscheff, M., Eberhard, D., Abraham, Y., Bastuck, S., Boesche, M., Hobson, S., Mathieson, T., Perrin, J., Raida, M., Rau, C., Reader, V., Sweetman, G., Bauer, A., Bouwmeester, T., Hopf, C., Kruse, U., Neubauer, G., Ramsden, N., Rick, J., Kuster, B., & Drewes, G. (2007). Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nature Biotechnology, 25(9), 1035–1044.

    Article  CAS  PubMed  Google Scholar 

  • Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., Verdu, E. F., & Collins, S. M. (2011). The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology, 141(2), 599–609, 609 e591–593.

    Article  CAS  PubMed  Google Scholar 

  • Berry, D., & Loy, A. (2018). Stable-isotope probing of human and animal microbiome function. Trends in Microbiology, 26(12), 999–1007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackburn, J. M., & Martens, L. (2016). The challenge of metaproteomic analysis in human samples. Expert Review of Proteomics, 13(2), 135–138.

    Article  CAS  PubMed  Google Scholar 

  • Blakeley-Ruiz, J. A., Erickson, A. R., Cantarel, B. L., Xiong, W., Adams, R., Jansson, J. K., Fraser, C. M., & Hettich, R. L. (2019). 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. Microbiome, 7(1), 18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Boersema, P. J., Raijmakers, R., Lemeer, S., Mohammed, S., & Heck, A. J. (2009). Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nature Protocols, 4(4), 484–494.

    Article  CAS  PubMed  Google Scholar 

  • Brooks, B., Mueller, R. S., Young, J. C., Morowitz, M. J., Hettich, R. L., & Banfield, J. F. (2015). Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant. Frontiers in Microbiology, 6, 654.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown, J. N., Ortiz, G. M., Angel, T. E., Jacobs, J. M., Gritsenko, M., Chan, E. Y., Purdy, D. E., Murnane, R. D., Larsen, K., Palermo, R. E., Shukla, A. K., Clauss, T. R., Katze, M. G., McCune, J. M., & Smith, R. D. (2012). Morphine produces immunosuppressive effects in nonhuman primates at the proteomic and cellular levels. Molecular & Cellular Proteomics, 11(9), 605–618.

    Article  CAS  Google Scholar 

  • Buchanan, J. M. (2002). Biochemistry during the life and times of Hans Krebs and Fritz Lipmann. The Journal of Biological Chemistry, 277(37), 33531–33536.

    Article  CAS  PubMed  Google Scholar 

  • Busch, R., Neese, R. A., Awada, M., Hayes, G. M., & Hellerstein, M. K. (2007). Measurement of cell proliferation by heavy water labeling. Nature Protocols, 2(12), 3045–3057.

    Article  CAS  PubMed  Google Scholar 

  • Cantarel, B. L., Erickson, A. R., VerBerkmoes, N. C., Erickson, B. K., Carey, P. A., Pan, C., Shah, M., Mongodin, E. F., Jansson, J. K., Fraser-Liggett, C. M., & Hettich, R. L. (2011). Strategies for metagenomic-guided whole-community proteomics of complex microbial environments. PLoS One, 6(11), e27173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carson, R. H., Lewis, C. R., Erickson, M. N., Zagieboylo, A. P., Naylor, B. C., Li, K. W., Farnsworth, P. B., & Price, J. C. (2017). Imaging regiospecific lipid turnover in mouse brain with desorption electrospray ionization mass spectrometry. Journal of Lipid Research, 58(9), 1884–1892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2013). The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Molecular Psychiatry, 18(6), 666–673.

    Article  CAS  PubMed  Google Scholar 

  • Claydon, A. J., & Beynon, R. (2012). Proteome dynamics: Revisiting turnover with a global perspective. Molecular & Cellular Proteomics, 11(12), 1551–1565.

    Article  CAS  Google Scholar 

  • Crumeyrolle-Arias, M., Jaglin, M., Bruneau, A., Vancassel, S., Cardona, A., Dauge, V., Naudon, L., & Rabot, S. (2014). Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology, 42, 207–217.

    Article  CAS  PubMed  Google Scholar 

  • David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., Biddinger, S. B., Dutton, R. J., & Turnbaugh, P. J. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505(7484), 559–563.

    Article  CAS  PubMed  Google Scholar 

  • Debyser, G., Mesuere, B., Clement, L., Van de Weygaert, J., Van Hecke, P., Duytschaever, G., Aerts, M., Dawyndt, P., De Boeck, K., Vandamme, P., & Devreese, B. (2016). Faecal proteomics: A tool to investigate dysbiosis and inflammation in patients with cystic fibrosis. Journal of Cystic Fibrosis, 15(2), 242–250.

    Article  CAS  PubMed  Google Scholar 

  • Decaris, M. L., Emson, C. L., Li, K., Gatmaitan, M., Luo, F., Cattin, J., Nakamura, C., Holmes, W. E., Angel, T. E., Peters, M. G., Turner, S. M., & Hellerstein, M. K. (2015). Turnover rates of hepatic collagen and circulating collagen-associated proteins in humans with chronic liver disease. PLoS One, 10(4), e0123311.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Decaris, M. L., Li, K. W., Emson, C. L., Gatmaitan, M., Liu, S., Wang, Y., Nyangau, E., Colangelo, M., Angel, T. E., Beysen, C., Cui, J., Hernandez, C., Lazaro, L., Brenner, D. A., Turner, S. M., Hellerstein, M. K., & Loomba, R. (2017). Identifying nonalcoholic fatty liver disease patients with active fibrosis by measuring extracellular matrix remodeling rates in tissue and blood. Hepatology, 65(1), 78–88.

    Article  CAS  PubMed  Google Scholar 

  • Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2014). Microbiota is essential for social development in the mouse. Molecular Psychiatry, 19(2), 146–148.

    Article  CAS  PubMed  Google Scholar 

  • Diamandis, E. P. (2012). The failure of protein cancer biomarkers to reach the clinic: Why, and what can be done to address the problem? BMC Medicine, 10, 87.

    Article  PubMed  PubMed Central  Google Scholar 

  • Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E., & Relman, D. A. (2005). Diversity of the human intestinal microbial flora. Science, 308(5728), 1635–1638.

    Article  PubMed  PubMed Central  Google Scholar 

  • Erickson, A. R., Cantarel, B. L., Lamendella, R., Darzi, Y., Mongodin, E. F., Pan, C., Shah, M., Halfvarson, J., Tysk, C., Henrissat, B., Raes, J., Verberkmoes, N. C., Fraser, C. M., Hettich, R. L., & Jansson, J. K. (2012). Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn’s disease. PLoS One, 7(11), e49138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrer, M., Ruiz, A., Lanza, F., Haange, S. B., Oberbach, A., Till, H., Bargiela, R., Campoy, C., Segura, M. T., Richter, M., von Bergen, M., Seifert, J., & Suarez, A. (2013). Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environmental Microbiology, 15(1), 211–226.

    Article  CAS  PubMed  Google Scholar 

  • Forslund, K., Sunagawa, S., Kultima, J. R., Mende, D. R., Arumugam, M., Typas, A., & Bork, P. (2013). Country-specific antibiotic use practices impact the human gut resistome. Genome Research, 23(7), 1163–1169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foster, J. A., Rinaman, L., & Cryan, J. F. (2017). Stress & the gut-brain axis: Regulation by the microbiome. Neurobiol Stress, 7, 124–136.

    Article  PubMed  PubMed Central  Google Scholar 

  • Garud, N. R., Good, B. H., Hallatschek, O., & Pollard, K. S. (2019). Evolutionary dynamics of bacteria in the gut microbiome within and across hosts. PLoS Biology, 17(1), e3000102.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gavin, P. G., Mullaney, J. A., Loo, D., Cao, K. L., Gottlieb, P. A., Hill, M. M., Zipris, D., & Hamilton-Williams, E. E. (2018). Intestinal Metaproteomics reveals host-microbiota interactions in subjects at risk for type 1 diabetes. Diabetes Care, 41(10), 2178–2186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerard, P. (2016). Gut microbiota and obesity. Cellular and Molecular Life Sciences, 73(1), 147–162.

    Article  CAS  PubMed  Google Scholar 

  • Goodrich, D. W., Wang, N. P., Qian, Y. W., Lee, E. Y., & Lee, W. H. (1991). The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle. Cell, 67(2), 293–302.

    Article  CAS  PubMed  Google Scholar 

  • Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J. T., Spector, T. D., Clark, A. G., & Ley, R. E. (2014). Human genetics shape the gut microbiome. Cell, 159(4), 789–799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordo, I. (2019). Evolutionary change in the human gut microbiome: From a static to a dynamic view. PLoS Biology, 17(2), e3000126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haange, S. B., Oberbach, A., Schlichting, N., Hugenholtz, F., Smidt, H., von Bergen, M., Till, H., & Seifert, J. (2012). Metaproteome analysis and molecular genetics of rat intestinal microbiota reveals section and localization resolved species distribution and enzymatic functionalities. Journal of Proteome Research, 11(11), 5406–5417.

    Article  CAS  PubMed  Google Scholar 

  • Hartman, A. L., Lough, D. M., Barupal, D. K., Fiehn, O., Fishbein, T., Zasloff, M., & Eisen, J. A. (2009). Human gut microbiome adopts an alternative state following small bowel transplantation. Proceedings of the National Academy of Sciences of the United States of America, 106(40), 17187–17192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hebert, A. S., Merrill, A. E., Bailey, D. J., Still, A. J., Westphall, M. S., Strieter, E. R., Pagliarini, D. J., & Coon, J. J. (2013). Neutron-encoded mass signatures for multiplexed proteome quantification. Nature Methods, 10(4), 332–334.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heintz-Buschart, A., May, P., Laczny, C. C., Lebrun, L. A., Bellora, C., Krishna, A., Wampach, L., Schneider, J. G., Hogan, A., de Beaufort, C., & Wilmes, P. (2016). Integrated multi-omics of the human gut microbiome in a case study of familial type 1 diabetes. Nature Microbiology, 2, 16180.

    Article  CAS  PubMed  Google Scholar 

  • Hellerstein, M. K. (2003). In vivo measurement of fluxes through metabolic pathways: The missing link in functional genomics and pharmaceutical research. Annual Review of Nutrition, 23, 379–402.

    Article  CAS  PubMed  Google Scholar 

  • Hellerstein, M. K., & Neese, R. A. (1992). Mass isotopomer distribution analysis: A technique for measuring biosynthesis and turnover of polymers. The American Journal of Physiology, 263(5 Pt 1), E988–E1001.

    CAS  PubMed  Google Scholar 

  • Hellerstein, M. K., & Neese, R. A. (1999). Mass isotopomer distribution analysis at eight years: Theoretical, analytic, and experimental considerations. The American Journal of Physiology, 276(6 Pt 1), E1146–E1170.

    CAS  PubMed  Google Scholar 

  • Hellerstein, M. K., Christiansen, M., Kaempfer, S., Kletke, C., Wu, K., Reid, J. S., Mulligan, K., Hellerstein, N. S., & Shackleton, C. H. (1991). Measurement of de novo hepatic lipogenesis in humans using stable isotopes. The Journal of Clinical Investigation, 87(5), 1841–1852.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez, E., Bargiela, R., Diez, M. S., Friedrichs, A., Perez-Cobas, A. E., Gosalbes, M. J., Knecht, H., Martinez-Martinez, M., Seifert, J., von Bergen, M., Artacho, A., Ruiz, A., Campoy, C., Latorre, A., Ott, S. J., Moya, A., Suarez, A., Martins dos Santos, V. A., & Ferrer, M. (2013). Functional consequences of microbial shifts in the human gastrointestinal tract linked to antibiotic treatment and obesity. Gut Microbes, 4(4), 306–315.

    Article  PubMed  PubMed Central  Google Scholar 

  • Holmes, W. E., Angel, T. E., Li, K. W., & Hellerstein, M. K. (2015). Dynamic proteomics: In vivo proteome-wide measurement of protein kinetics using metabolic labeling. Methods in Enzymology, 561, 219–276.

    Article  CAS  PubMed  Google Scholar 

  • Human Microbiome Project Consortium. (2012). Structure, function and diversity of the healthy human microbiome. Nature, 486(7402), 207–214.

    Article  CAS  Google Scholar 

  • Jones, P. J., & Leatherdale, S. T. (1991). Stable isotopes in clinical research: Safety reaffirmed. Clinical Science (London, England), 80(4), 277–280.

    Article  CAS  Google Scholar 

  • Juste, C., Kreil, D. P., Beauvallet, C., Guillot, A., Vaca, S., Carapito, C., Mondot, S., Sykacek, P., Sokol, H., Blon, F., Lepercq, P., Levenez, F., Valot, B., Carre, W., Loux, V., Pons, N., David, O., Schaeffer, B., Lepage, P., Martin, P., Monnet, V., Seksik, P., Beaugerie, L., Ehrlich, S. D., Gibrat, J. F., Van Dorsselaer, A., & Dore, J. (2014). Bacterial protein signals are associated with Crohn’s disease. Gut, 63(10), 1566–1577.

    Article  CAS  PubMed  Google Scholar 

  • Karlsson, F., Tremaroli, V., Nielsen, J., & Backhed, F. (2013). Assessing the human gut microbiota in metabolic diseases. Diabetes, 62(10), 3341–3349.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keshishian, H., Burgess, M. W., Specht, H., Wallace, L., Clauser, K. R., Gillette, M. A., & Carr, S. A. (2017). Quantitative, multiplexed workflow for deep analysis of human blood plasma and biomarker discovery by mass spectrometry. Nature Protocols, 12(8), 1683–1701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klaassens, E. S., de Vos, W. M., & Vaughan, E. E. (2007). Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract. Applied and Environmental Microbiology, 73(4), 1388–1392.

    Article  CAS  PubMed  Google Scholar 

  • Klimmeck, D., Hansson, J., Raffel, S., Vakhrushev, S. Y., Trumpp, A., & Krijgsveld, J. (2012). Proteomic cornerstones of hematopoietic stem cell differentiation: Distinct signatures of multipotent progenitors and myeloid committed cells. Molecular & Cellular Proteomics, 11(8), 286–302.

    Article  CAS  Google Scholar 

  • Kolmeder, C. A., & de Vos, W. M. (2014). Metaproteomics of our microbiome – developing insight in function and activity in man and model systems. Journal of Proteomics, 97, 3–16.

    Article  CAS  PubMed  Google Scholar 

  • Kolmeder, C. A., de Been, M., Nikkila, J., Ritamo, I., Matto, J., Valmu, L., Salojarvi, J., Palva, A., Salonen, A., & de Vos, W. M. (2012). Comparative metaproteomics and diversity analysis of human intestinal microbiota testifies for its temporal stability and expression of core functions. PLoS One, 7(1), e29913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolmeder, C. A., Salojarvi, J., Ritari, J., de Been, M., Raes, J., Falony, G., Vieira-Silva, S., Kekkonen, R. A., Corthals, G. L., Palva, A., Salonen, A., & de Vos, W. M. (2016). Faecal metaproteomic analysis reveals a personalized and stable functional microbiome and limited effects of a probiotic intervention in adults. PLoS One, 11(4), e0153294.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kristensen, N. B., Bryrup, T., Allin, K. H., Nielsen, T., Hansen, T. H., & Pedersen, O. (2016). Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: A systematic review of randomized controlled trials. Genome Medicine, 8(1), 52.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lam, M. P., Wang, D., Lau, E., Liem, D. A., Kim, A. K., Ng, D. C., Liang, X., Bleakley, B. J., Liu, C., Tabaraki, J. D., Cadeiras, M., Wang, Y., Deng, M. C., & Ping, P. (2014). Protein kinetic signatures of the remodeling heart following isoproterenol stimulation. The Journal of Clinical Investigation, 124(4), 1734–1744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, P. Y., Chin, S. F., Neoh, H. M., & Jamal, R. (2017). Metaproteomic analysis of human gut microbiota: Where are we heading? Journal of Biomedical Science, 24(1), 36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmann, T., Schallert, K., Vilchez-Vargas, R., Benndorf, D., Puttker, S., Sydor, S., Schulz, C., Bechmann, L., Canbay, A., Heidrich, B., Reichl, U., Link, A., & Heyer, R. (2019). Metaproteomics of fecal samples of Crohn’s disease and ulcerative colitis. Journal of Proteomics, 201, 93–103.

    Article  CAS  PubMed  Google Scholar 

  • Ley, R. E., Backhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., & Gordon, J. I. (2005). Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America, 102(31), 11070–11075.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ley, R. E., Turnbaugh, P. J., Klein, S., & Gordon, J. I. (2006). Microbial ecology: Human gut microbes associated with obesity. Nature, 444(7122), 1022–1023.

    Article  CAS  PubMed  Google Scholar 

  • Li, X., LeBlanc, J., Truong, A., Vuthoori, R., Chen, S. S., Lustgarten, J. L., Roth, B., Allard, J., Ippoliti, A., Presley, L. L., Borneman, J., Bigbee, W. L., Gopalakrishnan, V., Graeber, T. G., Elashoff, D., Braun, J., & Goodglick, L. (2011). A metaproteomic approach to study human-microbial ecosystems at the mucosal luminal interface. PLoS One, 6(11), e26542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, L., Zhang, X., Ning, Z., Mayne, J., Moore, J. I., Butcher, J., Chiang, C. K., Mack, D., Stintzi, A., & Figeys, D. (2018). Evaluating in vitro culture medium of gut microbiome with orthogonal experimental design and a metaproteomics approach. Journal of Proteome Research, 17(1), 154–163.

    Article  CAS  PubMed  Google Scholar 

  • Liu, C. W., Chi, L., Tu, P., Xue, J., Ru, H., & Lu, K. (2019). Isobaric labeling quantitative metaproteomics for the study of gut microbiome response to arsenic. Journal of Proteome Research, 18(3), 970–981.

    Article  CAS  PubMed  Google Scholar 

  • Lloyd-Price, J., Mahurkar, A., Rahnavard, G., Crabtree, J., Orvis, J., Hall, A. B., Brady, A., Creasy, H. H., McCracken, C., Giglio, M. G., McDonald, D., Franzosa, E. A., Knight, R., White, O., & Huttenhower, C. (2017). Strains, functions and dynamics in the expanded Human Microbiome Project. Nature, 550(7674), 61–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lundberg, E., & Borner, G. H. H. (2019). Spatial proteomics: A powerful discovery tool for cell biology. Nature Reviews. Molecular Cell Biology, 20(5), 285–302.

    Article  CAS  PubMed  Google Scholar 

  • Lynch, S. V., Ng, S. C., Shanahan, F., & Tilg, H. (2019). Translating the gut microbiome: Ready for the clinic? Nature Reviews. Gastroenterology & Hepatology, 16(11), 656–661.

    Article  Google Scholar 

  • Matsuoka, K., & Kanai, T. (2015). The gut microbiota and inflammatory bowel disease. Seminars in Immunopathology, 37(1), 47–55.

    Article  CAS  PubMed  Google Scholar 

  • McBride, Z., Chen, D., Lee, Y., Aryal, U. K., Xie, J., & Szymanski, D. B. (2019). A label-free mass spectrometry method to predict endogenous protein complex composition. Molecular & Cellular Proteomics, 18, 1588–1606.

    Article  CAS  Google Scholar 

  • Meier, F., Brunner, A. D., Koch, S., Koch, H., Lubeck, M., Krause, M., Goedecke, N., Decker, J., Kosinski, T., Park, M. A., Bache, N., Hoerning, O., Cox, J., Rather, O., & Mann, M. (2018). Online parallel accumulation-serial fragmentation (PASEF) with a novel trapped ion mobility mass spectrometer. Molecular & Cellular Proteomics, 17(12), 2533–2545.

    Article  Google Scholar 

  • Merrill, A. E., Hebert, A. S., MacGilvray, M. E., Rose, C. M., Bailey, D. J., Bradley, J. C., Wood, W. W., El Masri, M., Westphall, M. S., Gasch, A. P., & Coon, J. J. (2014). NeuCode labels for relative protein quantification. Molecular & Cellular Proteomics, 13(9), 2503–2512.

    Article  CAS  Google Scholar 

  • Mertins, P., Udeshi, N. D., Clauser, K. R., Mani, D. R., Patel, J., Ong, S. E., Jaffe, J. D., & Carr, S. A. (2012). iTRAQ labeling is superior to mTRAQ for quantitative global proteomics and phosphoproteomics. Molecular & Cellular Proteomics, 11(6), M111 014423.

    Article  CAS  Google Scholar 

  • Moeller, A. H., Li, Y., Mpoudi Ngole, E., Ahuka-Mundeke, S., Lonsdorf, E. V., Pusey, A. E., Peeters, M., Hahn, B. H., & Ochman, H. (2014). Rapid changes in the gut microbiome during human evolution. Proceedings of the National Academy of Sciences of the United States of America, 111(46), 16431–16435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moeller, A. H., Caro-Quintero, A., Mjungu, D., Georgiev, A. V., Lonsdorf, E. V., Muller, M. N., Pusey, A. E., Peeters, M., Hahn, B. H., & Ochman, H. (2016). Cospeciation of gut microbiota with hominids. Science, 353(6297), 380–382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohajeri, M. H., La Fata, G., Steinert, R. E., & Weber, P. (2018). Relationship between the gut microbiome and brain function. Nutrition Reviews, 76(7), 481–496.

    Article  PubMed  Google Scholar 

  • Moulder, R., Bhosale, S. D., Goodlett, D. R., & Lahesmaa, R. (2018). Analysis of the plasma proteome using iTRAQ and TMT-based isobaric labeling. Mass Spectrometry Reviews, 37(5), 583–606.

    Article  CAS  PubMed  Google Scholar 

  • Munoz, J., Stange, D. E., Schepers, A. G., van de Wetering, M., Koo, B. K., Itzkovitz, S., Volckmann, R., Kung, K. S., Koster, J., Radulescu, S., Myant, K., Versteeg, R., Sansom, O. J., van Es, J. H., Barker, N., van Oudenaarden, A., Mohammed, S., Heck, A. J., & Clevers, H. (2012). The Lgr5 intestinal stem cell signature: Robust expression of proposed quiescent ‘+4’ cell markers. The EMBO Journal, 31(14), 3079–3091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munson, M. A., Baumann, P., Clark, M. A., Baumann, L., Moran, N. A., Voegtlin, D. J., & Campbell, B. C. (1991). Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. Journal of Bacteriology, 173(20), 6321–6324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muth, T., Behne, A., Heyer, R., Kohrs, F., Benndorf, D., Hoffmann, M., Lehteva, M., Reichl, U., Martens, L., & Rapp, E. (2015). The MetaProteomeAnalyzer: A powerful open-source software suite for metaproteomics data analysis and interpretation. Journal of Proteome Research, 14(3), 1557–1565.

    Article  CAS  PubMed  Google Scholar 

  • Muth, T., Renard, B. Y., & Martens, L. (2016). Metaproteomic data analysis at a glance: Advances in computational microbial community proteomics. Expert Review of Proteomics, 13(8), 757–769.

    Article  CAS  PubMed  Google Scholar 

  • Naylor, B. C., Porter, M. T., Wilson, E., Herring, A., Lofthouse, S., Hannemann, A., Piccolo, S. R., Rockwood, A. L., & Price, J. C. (2017). DeuteRater: A tool for quantifying peptide isotope precision and kinetic proteomics. Bioinformatics, 33(10), 1514–1520.

    CAS  PubMed  Google Scholar 

  • Neese, R. A., Schwarz, J. M., Faix, D., Turner, S., Letscher, A., Vu, D., & Hellerstein, M. K. (1995). Gluconeogenesis and intrahepatic triose phosphate flux in response to fasting or substrate loads. Application of the mass isotopomer distribution analysis technique with testing of assumptions and potential problems. The Journal of Biological Chemistry, 270(24), 14452–14466.

    Article  CAS  PubMed  Google Scholar 

  • Nolting, D., Malek, R., & Makarov, A. (2017). Ion traps in modern mass spectrometry. Mass Spectrometry Reviews, 38, 150–168.

    Article  PubMed  CAS  Google Scholar 

  • Ochman, H., Worobey, M., Kuo, C. H., Ndjango, J. B., Peeters, M., Hahn, B. H., & Hugenholtz, P. (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biology, 8(11), e1000546.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins. The Journal of Biological Chemistry, 250(10), 4007–4021.

    Article  PubMed  Google Scholar 

  • Ogbonnaya, E. S., Clarke, G., Shanahan, F., Dinan, T. G., Cryan, J. F., & O’Leary, O. F. (2015). Adult hippocampal neurogenesis is regulated by the microbiome. Biological Psychiatry, 78(4), e7–e9.

    Article  PubMed  Google Scholar 

  • Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., & Mann, M. (2002). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Molecular & Cellular Proteomics, 1(5), 376–386.

    Article  CAS  Google Scholar 

  • Overmyer, K. A., Tyanova, S., Hebert, A. S., Westphall, M. S., Cox, J., & Coon, J. J. (2018). Multiplexed proteome analysis with neutron-encoded stable isotope labeling in cells and mice. Nature Protocols, 13(1), 293–306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paulovich, A. G., Whiteaker, J. R., Hoofnagle, A. N., & Wang, P. (2008). The interface between biomarker discovery and clinical validation: The tar pit of the protein biomarker pipeline. Proteomics. Clinical Applications, 2(10–11), 1386–1402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Percy, A. J., Byrns, S., Pennington, S. R., Holmes, D. T., Anderson, N. L., Agreste, T. M., & Duffy, M. A. (2016). Clinical translation of MS-based, quantitative plasma proteomics: Status, challenges, requirements, and potential. Expert Review of Proteomics, 13(7), 673–684.

    Article  CAS  PubMed  Google Scholar 

  • Perez-Cobas, A. E., Artacho, A., Knecht, H., Ferrus, M. L., Friedrichs, A., Ott, S. J., Moya, A., Latorre, A., & Gosalbes, M. J. (2013a). Differential effects of antibiotic therapy on the structure and function of human gut microbiota. PLoS One, 8(11), e80201.

    Article  PubMed  PubMed Central  Google Scholar 

  • Perez-Cobas, A. E., Gosalbes, M. J., Friedrichs, A., Knecht, H., Artacho, A., Eismann, K., Otto, W., Rojo, D., Bargiela, R., von Bergen, M., Neulinger, S. C., Daumer, C., Heinsen, F. A., Latorre, A., Barbas, C., Seifert, J., dos Santos, V. M., Ott, S. J., Ferrer, M., & Moya, A. (2013b). Gut microbiota disturbance during antibiotic therapy: A multi-omic approach. Gut, 62(11), 1591–1601.

    Article  CAS  PubMed  Google Scholar 

  • Pfammatter, S., Bonneil, E., McManus, F. P., Prasad, S., Bailey, D. J., Belford, M., Dunyach, J.-J., & Thibault, P. (2018). A novel differential ion mobility device expands the depth of proteome coverage and the sensitivity of multiplex proteomic measurements. Molecular & Cellular Proteomics, 17(10), 2051–2067.

    Article  CAS  Google Scholar 

  • Presley, L. L., Ye, J., Li, X., Leblanc, J., Zhang, Z., Ruegger, P. M., Allard, J., McGovern, D., Ippoliti, A., Roth, B., Cui, X., Jeske, D. R., Elashoff, D., Goodglick, L., Braun, J., & Borneman, J. (2012). Host-microbe relationships in inflammatory bowel disease detected by bacterial and metaproteomic analysis of the mucosal-luminal interface. Inflammatory Bowel Diseases, 18(3), 409–417.

    Article  PubMed  Google Scholar 

  • Price, J. C., Guan, S., Burlingame, A., Prusiner, S. B., & Ghaemmaghami, S. (2010). Analysis of proteome dynamics in the mouse brain. Proceedings of the National Academy of Sciences of the United States of America, 107(32), 14508–14513.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price, J. C., Holmes, W. E., Li, K. W., Floreani, N. A., Neese, R. A., Turner, S. M., & Hellerstein, M. K. (2012a). Measurement of human plasma proteome dynamics with (2)H(2)O and liquid chromatography tandem mass spectrometry. Analytical Biochemistry, 420(1), 73–83.

    Article  CAS  PubMed  Google Scholar 

  • Price, J. C., Khambatta, C. F., Li, K. W., Bruss, M. D., Shankaran, M., Dalidd, M., Floreani, N. A., Roberts, L. S., Turner, S. M., Holmes, W. E., & Hellerstein, M. K. (2012b). The effect of long term calorie restriction on in vivo hepatic proteostatis: A novel combination of dynamic and quantitative proteomics. Molecular & Cellular Proteomics, 11(12), 1801–1814.

    Article  CAS  Google Scholar 

  • Price, R. W., Peterson, J., Fuchs, D., Angel, T. E., Zetterberg, H., Hagberg, L., Spudich, S., Smith, R. D., Jacobs, J. M., Brown, J. N., & Gisslen, M. (2013). Approach to cerebrospinal fluid (CSF) biomarker discovery and evaluation in HIV infection. Journal of Neuroimmune Pharmacology, 8(5), 1147–1158.

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., Mende, D. R., Li, J., Xu, J., Li, S., Li, D., Cao, J., Wang, B., Liang, H., Zheng, H., Xie, Y., Tap, J., Lepage, P., Bertalan, M., Batto, J. M., Hansen, T., Le Paslier, D., Linneberg, A., Nielsen, H. B., Pelletier, E., Renault, P., Sicheritz-Ponten, T., Turner, K., Zhu, H., Yu, C., Li, S., Jian, M., Zhou, Y., Li, Y., Zhang, X., Li, S., Qin, N., Yang, H., Wang, J., Brunak, S., Dore, J., Guarner, F., Kristiansen, K., Pedersen, O., Parkhill, J., Weissenbach, J., Meta, H. I. T. C., Bork, P., Ehrlich, S. D., & Wang, J. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464(7285), 59–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoads, T. W., Rose, C. M., Bailey, D. J., Riley, N. M., Molden, R. C., Nestler, A. J., Merrill, A. E., Smith, L. M., Hebert, A. S., Westphall, M. S., Pagliarini, D. J., Garcia, B. A., & Coon, J. J. (2014). Neutron-encoded mass signatures for quantitative top-down proteomics. Analytical Chemistry, 86(5), 2314–2319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richards, A. L., Vincent, C. E., Guthals, A., Rose, C. M., Westphall, M. S., Bandeira, N., & Coon, J. J. (2013). Neutron-encoded signatures enable product ion annotation from tandem mass spectra. Molecular & Cellular Proteomics, 12(12), 3812–3823.

    Article  CAS  Google Scholar 

  • Saji, N., Niida, S., Murotani, K., Hisada, T., Tsuduki, T., Sugimoto, T., Kimura, A., Toba, K., & Sakurai, T. (2019). Analysis of the relationship between the gut microbiome and dementia: A cross-sectional study conducted in Japan. Scientific Reports, 9(1), 1008.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Savitski, M. M., Zinn, N., Faelth-Savitski, M., Poeckel, D., Gade, S., Becher, I., Muelbaier, M., Wagner, A. J., Strohmer, K., Werner, T., Melchert, S., Petretich, M., Rutkowska, A., Vappiani, J., Franken, H., Steidel, M., Sweetman, G. M., Gilan, O., Lam, E. Y. N., Dawson, M. A., Prinjha, R. K., Grandi, P., Bergamini, G., & Bantscheff, M. (2018). Multiplexed proteome dynamics profiling reveals mechanisms controlling protein homeostasis. Cell, 173(1), 260–274 e225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss, P. D., Iverson, K. D., Petrosino, J. F., & Schloss, S. J. (2014). The dynamics of a family’s gut microbiota reveal variations on a theme. Microbiome, 2, 25.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schoenheimer, R., & Rittenberg, D. (1936). Deuterium as an indicator in the study of intermediary metabolism: VI. Synthesis and destruction of fatty acids in the organism. Journal of Biological Chemistry, 114(2), 381–396.

    Article  CAS  Google Scholar 

  • Schutzer, S. E., Liu, T., Natelson, B. H., Angel, T. E., Schepmoes, A. A., Purvine, S. O., Hixson, K. K., Lipton, M. S., Camp, D. G., Coyle, P. K., Smith, R. D., & Bergquist, J. (2010). Establishing the proteome of normal human cerebrospinal fluid. PLoS One, 5(6), e10980.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schutzer, S. E., Angel, T. E., Liu, T., Schepmoes, A. A., Clauss, T. R., Adkins, J. N., Camp, D. G., Holland, B. K., Bergquist, J., Coyle, P. K., Smith, R. D., Fallon, B. A., & Natelson, B. H. (2011). Distinct cerebrospinal fluid proteomes differentiate post-treatment Lyme disease from chronic fatigue syndrome. PLoS One, 6(2), e17287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schutzer, S. E., Angel, T. E., Liu, T., Schepmoes, A. A., Xie, F., Bergquist, J., Vecsei, L., Zadori, D., Camp, D. G., 2nd, Holland, B. K., Smith, R. D., & Coyle, P. K. (2013). Gray matter is targeted in first-attack multiple sclerosis. PLoS One, 8(9), e66117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwanhausser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011). Global quantification of mammalian gene expression control. Nature, 473(7347), 337–342.

    Article  PubMed  CAS  Google Scholar 

  • Sender, R., Fuchs, S., & Milo, R. (2016). Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14(8), e1002533.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shankaran, M., King, C. L., Angel, T. E., Holmes, W. E., Li, K. W., Colangelo, M., Price, J. C., Turner, S. M., Bell, C., Hamilton, K. L., Miller, B. F., & Hellerstein, M. K. (2016). Circulating protein synthesis rates reveal skeletal muscle proteome dynamics. The Journal of Clinical Investigation, 126(1), 288–302.

    Article  PubMed  Google Scholar 

  • Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016). The central nervous system and the gut microbiome. Cell, 167(4), 915–932.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slebos, R. J., Brock, J. W., Winters, N. F., Stuart, S. R., Martinez, M. A., Li, M., Chambers, M. C., Zimmerman, L. J., Ham, A. J., & Tabb, D. L. (2008). Evaluation of strong cation exchange versus isoelectric focusing of peptides for multidimensional liquid chromatography-tandem mass spectrometry. Journal of Proteome Research, 7(12), 5286–5294.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, L. M., Kelleher, N. L., & Consortium for Top Down Proteomics. (2013). Proteoform: A single term describing protein complexity. Nature Methods, 10(3), 186–187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, J. S., Angel, T. E., Chavkin, C., Orton, D. J., Moore, R. J., & Smith, R. D. (2014). Characterization of individual mouse cerebrospinal fluid proteomes. Proteomics, 14(9), 1102–1106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, S. J., Lauber, C., Costello, E. K., Lozupone, C. A., Humphrey, G., Berg-Lyons, D., Caporaso, J. G., Knights, D., Clemente, J. C., Nakielny, S., Gordon, J. I., Fierer, N., & Knight, R. (2013). Cohabiting family members share microbiota with one another and with their dogs. eLife, 2, e00458.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanca, A., Palomba, A., Pisanu, S., Addis, M. F., & Uzzau, S. (2015). Enrichment or depletion? The impact of stool pretreatment on metaproteomic characterization of the human gut microbiota. Proteomics, 15(20), 3474–3485.

    Article  CAS  PubMed  Google Scholar 

  • Timmins-Schiffman, E., May, D. H., Mikan, M., Riffle, M., Frazar, C., Harvey, H. R., Noble, W. S., & Nunn, B. L. (2017). Critical decisions in metaproteomics: Achieving high confidence protein annotations in a sea of unknowns. The ISME Journal, 11(2), 309–314.

    Article  CAS  PubMed  Google Scholar 

  • Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444(7122), 1027–1031.

    Article  PubMed  Google Scholar 

  • Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R., & Gordon, J. I. (2007). The human microbiome project. Nature, 449(7164), 804–810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R., & Gordon, J. I. (2009). The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Science Translational Medicine, 1(6), 6ra14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Turner, S. M., & Hellerstein, M. K. (2005). Emerging applications of kinetic biomarkers in preclinical and clinical drug development. Current Opinion in Drug Discovery & Development, 8(1), 115–126.

    CAS  Google Scholar 

  • Verberkmoes, N. C., Russell, A. L., Shah, M., Godzik, A., Rosenquist, M., Halfvarson, J., Lefsrud, M. G., Apajalahti, J., Tysk, C., Hettich, R. L., & Jansson, J. K. (2009). Shotgun metaproteomics of the human distal gut microbiota. The ISME Journal, 3(2), 179–189.

    Article  CAS  PubMed  Google Scholar 

  • Voogt, J. N., Awada, M., Murphy, E. J., Hayes, G. M., Busch, R., & Hellerstein, M. K. (2007). Measurement of very low rates of cell proliferation by heavy water labeling of DNA and gas chromatography/pyrolysis/isotope ratio-mass spectrometric analysis. Nature Protocols, 2(12), 3058–3062.

    Article  CAS  PubMed  Google Scholar 

  • Wei, X., Jiang, S., Chen, Y., Zhao, X., Li, H., Lin, W., Li, B., Wang, X., Yuan, J., & Sun, Y. (2016). Cirrhosis related functionality characteristic of the fecal microbiota as revealed by a metaproteomic approach. BMC Gastroenterology, 16(1), 121.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Welle, K. A., Zhang, T., Hryhorenko, J. R., Shen, S., Qu, J., & Ghaemmaghami, S. (2016). Time-resolved analysis of proteome dynamics by tandem mass tags and stable isotope labeling in cell culture (TMT-SILAC) hyperplexing. Molecular & Cellular Proteomics, 15(12), 3551–3563.

    Article  CAS  Google Scholar 

  • Wong, M. L., Inserra, A., Lewis, M. D., Mastronardi, C. A., Leong, L., Choo, J., Kentish, S., Xie, P., Morrison, M., Wesselingh, S. L., Rogers, G. B., & Licinio, J. (2016). Inflammasome signaling affects anxiety- and depressive-like behavior and gut microbiome composition. Molecular Psychiatry, 21(6), 797–805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong, W., Abraham, P. E., Li, Z., Pan, C., & Hettich, R. L. (2015). Microbial metaproteomics for characterizing the range of metabolic functions and activities of human gut microbiota. Proteomics, 15(20), 3424–3438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, F., Shen, Y., Camp, D. G., & Smith, R. D. (2012). High-pH reversed-phase chromatography with fraction concatenation for 2D proteomic analysis. Expert Review of Proteomics, 9(2), 129–134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., Heath, A. C., Warner, B., Reeder, J., Kuczynski, J., Caporaso, J. G., Lozupone, C. A., Lauber, C., Clemente, J. C., Knights, D., Knight, R., & Gordon, J. I. (2012). Human gut microbiome viewed across age and geography. Nature, 486(7402), 222–227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young, J. C., Pan, C., Adams, R. M., Brooks, B., Banfield, J. F., Morowitz, M. J., & Hettich, R. L. (2015). Metaproteomics reveals functional shifts in microbial and human proteins during a preterm infant gut colonization case. Proteomics, 15(20), 3463–3473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young, P. A., Leonard, S., Martin, D. S., & Findlay, J. B. (2016). Analysis of the effect of a novel therapeutic for type 2 diabetes on the proteome of a muscle cell line. Proteomics, 16(1), 70–79.

    Article  CAS  PubMed  Google Scholar 

  • Zecha, J., Meng, C., Zolg, D. P., Samaras, P., Wilhelm, M., & Kuster, B. (2018). Peptide level turnover measurements enable the study of proteoform dynamics. Molecular & Cellular Proteomics, 17(5), 974–992.

    Article  CAS  Google Scholar 

  • Zhang, X., Ning, Z., Mayne, J., Moore, J. I., Li, J., Butcher, J., Deeke, S. A., Chen, R., Chiang, C. K., Wen, M., Mack, D., Stintzi, A., & Figeys, D. (2016). MetaPro-IQ: A universal metaproteomic approach to studying human and mouse gut microbiota. Microbiome, 4(1), 31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, X., Deeke, S. A., Ning, Z., Starr, A. E., Butcher, J., Li, J., Mayne, J., Cheng, K., Liao, B., Li, L., Singleton, R., Mack, D., Stintzi, A., & Figeys, D. (2018a). Metaproteomics reveals associations between microbiome and intestinal extracellular vesicle proteins in pediatric inflammatory bowel disease. Nature Communications, 9(1), 2873.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang, X., Li, L., Mayne, J., Ning, Z., Stintzi, A., & Figeys, D. (2018b). Assessing the impact of protein extraction methods for human gut metaproteomics. Journal of Proteomics, 180, 120–127.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, X., Wojcik, R., Zhang, X., Ibrahim, Y. M., Burnum-Johnson, K. E., Orton, D. J., Monroe, M. E., Moore, R. J., Smith, R. D., & Baker, E. S. (2017). Coupling front-end separations, ion mobility spectrometry, and mass spectrometry for enhanced multidimensional biological and environmental analyses. Annual Review of Analytical Chemistry (Palo Alto, California), 10(1), 71–92.

    Article  CAS  Google Scholar 

  • Zou, Y., Xue, W., Luo, G., Deng, Z., Qin, P., Guo, R., Sun, H., Xia, Y., Liang, S., Dai, Y., Wan, D., Jiang, R., Su, L., Feng, Q., Jie, Z., Guo, T., Xia, Z., Liu, C., Yu, J., Lin, Y., Tang, S., Huo, G., Xu, X., Hou, Y., Liu, X., Wang, J., Yang, H., Kristiansen, K., Li, J., Jia, H., & Xiao, L. (2019). 1,520 reference genomes from cultivated human gut bacteria enable functional microbiome analyses. Nature Biotechnology, 37(2), 179–185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwittink, R. D., van Zoeren-Grobben, D., Martin, R., van Lingen, R. A., Groot Jebbink, L. J., Boeren, S., Renes, I. B., van Elburg, R. M., Belzer, C., & Knol, J. (2017). Metaproteomics reveals functional differences in intestinal microbiota development of preterm infants. Molecular & Cellular Proteomics, 16(9), 1610–1620.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas E. Angel .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Angel, T.E., Aryal, U.K. (2020). Impact of Gut Microbiota on Host by Exploring Proteomics. In: Biswas, D., Rahaman, S.O. (eds) Gut Microbiome and Its Impact on Health and Diseases. Springer, Cham. https://doi.org/10.1007/978-3-030-47384-6_11

Download citation

Publish with us

Policies and ethics