Applied Microbiology and Biotechnology

, Volume 101, Issue 8, pp 3077–3088 | Cite as

Metaproteomic strategies and applications for gut microbial research

  • Mingming Xiao
  • Junjun Yang
  • Yuxin Feng
  • Yan Zhu
  • Xin Chai
  • Yuefei Wang
Mini-Review

Abstract

The human intestine hosts various complex microbial communities that are closely associated with multiple health and disease processes. Determining the composition and function of these microbial communities is critical to unveil disease mechanisms and promote human health. Recently, meta-omic strategies have been developed that use high-throughput techniques to provide a wealth of information, thus accelerating the study of gut microbes. Metaproteomics is a newly emerged analytical approach that aims to identify proteins on a large scale in complex environmental microbial communities (e.g., the gut microbiota). This review introduces the recent analytical strategies and applications of metaproteomics, with a focus on advances in gut microbiota research, including a discussion of the limitations and challenges of these approaches.

Keywords

Metaproteomics Gut microbiota Application Protein identification Mass spectrometry 

References

  1. Aires J, Butel MJ (2011) Proteomics, human gut microbiota and probiotics. Expert Rev Proteomics 8(2):279–288. doi:10.1586/epr.11.5 CrossRefPubMedGoogle Scholar
  2. Apajalahti JH, Sarkilahti LK, Maki BR, Heikkinen JP, Nurminen PH, Holben WE (1998) Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Appl Environ Microbiol 64(10):4084–4088PubMedPubMedCentralGoogle Scholar
  3. Bai Z, Zhang H, Li N, Bai Z, Zhang L, Xue Z, Jiang H, Song Y, Zhou D (2016) Impact of environmental microbes on the composition of the gut microbiota of adult BALB/c mice. PLoS One 11(8):e0160568. doi:10.1371/journal.pone.0160568 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baothman OA, Zamzami MA, Taher I, Abubaker J, Abu-Farha M (2016) The role of gut microbiota in the development of obesity and diabetes. Lipids Health Dis 15:108. doi:10.1186/s12944-016-0278-4 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Barker CJ, Gillett A, Polkinghorne A, Timms P (2013) Investigation of the koala (Phascolarctos cinereus) hindgut microbiome via 16S pyrosequencing. Vet Microbiol 167(3–4):554–564. doi:10.1016/j.vetmic.2013.08.025 CrossRefPubMedGoogle Scholar
  6. Betancourt LH, De Bock PJ, Staes A, Timmerman E, Perez-Riverol Y, Sanchez A, Besada V, Gonzalez LJ, Vandekerckhove J, Gevaert K (2013) SCX charge state selective separation of tryptic peptides combined with 2D-RP-HPLC allows for detailed proteome mapping. J Proteome 91:164–171. doi:10.1016/j.jprot.2013.06.033 CrossRefGoogle Scholar
  7. Bohm R, Cascorbi I (2016) Pharmacogenetics and predictive testing of drug hypersensitivity reactions. Front Pharmacol 7:396. doi:10.3389/fphar.2016.00396 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bojanova DP, Bordenstein SR (2016) Fecal transplants: what is being transferred? PLoS Biol 14(7):e1002503. doi:10.1371/journal.pbio.1002503 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brooks B, Mueller RS, Young JC, Morowitz MJ, Hettich RL, Banfield JF (2015) Strain-resolved microbial community proteomics reveals simultaneous aerobic and anaerobic function during gastrointestinal tract colonization of a preterm infant. Front Microbiol 6:654. doi:10.3389/fmicb.2015.00654 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brunelle JL, Green R (2014) One-dimensional SDS-polyacrylamide gel electrophoresis (1D SDS-PAGE). Methods Enzymol 541:151–159. doi:10.1016/B978-0-12-420119-4.00012-4 CrossRefPubMedGoogle Scholar
  11. Bugianesi E (2005) Review article: steatosis, the metabolic syndrome and cancer. Aliment Pharmacol Ther Suppl 2:40–43. doi:10.1111/j.1365-2036.2005.02594.x CrossRefGoogle Scholar
  12. Caprioli RM, Farmer TB, Gile J (1997) Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS. Anal Chem 69(23):4751–4760CrossRefPubMedGoogle Scholar
  13. Carrasco-Navarro U, Vera-Estrella R, Barkla BJ, Zuniga-Leon E, Reyes-Vivas H, Fernandez FJ, Fierro F (2016) Proteomic analysis of the signaling pathway mediated by the heterotrimeric Galpha protein Pga1 of Penicillium chrysogenum. Microb Cell Factories 15(1):173. doi:10.1186/s12934-016-0564-x CrossRefGoogle Scholar
  14. Chen R, Xiao M, Gao H, Chen Y, Li Y, Liu Y, Zhang N (2016) Identification of a novel mitochondrial interacting protein of C1QBP using subcellular fractionation coupled with CoIP-MS. Anal Bioanal Chem 408(6):1557–1564. doi:10.1007/s00216-015-9228-7 CrossRefPubMedGoogle Scholar
  15. Cheruthazhekatt S, Harding GW, Pasch H (2013) Comprehensive high temperature two-dimensional liquid chromatography combined with high temperature gradient chromatography-infrared spectroscopy for the analysis of impact polypropylene copolymers. J Chromatogr A 1286:69–82. doi:10.1016/j.chroma.2013.02.052 CrossRefPubMedGoogle Scholar
  16. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326(5960):1694–1697. doi:10.1126/science.1177486 CrossRefPubMedPubMedCentralGoogle Scholar
  17. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563. doi:10.1038/nature12820 CrossRefPubMedGoogle Scholar
  18. Del Chierico F, Petrucca A, Mortera SL, Vernocchi P, Rosado MM, Pieroni L, Carsetti R, Urbani A, Putignani L (2014) A metaproteomic pipeline to identify newborn mouse gut phylotypes. J Proteome 97:17–26. doi:10.1016/j.jprot.2013.10.025 CrossRefGoogle Scholar
  19. Dhabaria A, Cifani P, Reed C, Steen H, Kentsis A (2015) A high-efficiency cellular extraction system for biological proteomics. J Proteome Res 14(8):3403–3408. doi:10.1021/acs.jproteome.5b00547 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, Bultman SJ (2011) The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 13(5):517–526. doi:10.1016/j.cmet.2011.02.018 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Douglas DJ, Frank AJ, Mao D (2005) Linear ion traps in mass spectrometry. Mass Spectrom Rev 24(1):1–29. doi:10.1002/mas.20004 CrossRefPubMedGoogle Scholar
  22. Dumpala PR, Lawrence ML, Karsi A (2009) Proteome analysis of Edwardsiella ictaluri. Proteomics 9(5):1353–1363. doi:10.1002/pmic.200800652 CrossRefPubMedGoogle Scholar
  23. Erickson AR, Cantarel BL, Lamendella R, Darzi Y, Mongodin EF, Pan C, Shah M, Halfvarson J, Tysk C, Henrissat B, Raes J, Verberkmoes NC, Fraser CM, Hettich RL, Jansson JK (2012) Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn’s disease. PLoS One 7(11):e49138. doi:10.1371/journal.pone.0049138 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ficarro SB, Zhang Y, Carrasco-Alfonso MJ, Garg B, Adelmant G, Webber JT, Luckey CJ, Marto JA (2011) Online nanoflow multidimensional fractionation for high efficiency phosphopeptide analysis. Mol Cell Proteomics 10(11):O111.011064. doi:10.1074/mcp.O111.011064 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gao G, Zhao X, Li Q, He C, Zhao W, Liu S, Ding J, Ye W, Wang J, Chen Y, Wang H, Li J, Luo Y, Su J, Huang Y, Liu Z, Dai R, Shi Y, Meng H, Wang Q (2016) Genome and metagenome analyses reveal adaptive evolution of the host and interaction with the gut microbiota in the goose. Sci Rep 6:32961. doi:10.1038/srep32961 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Graf D, Di Cagno R, Fak F, Flint HJ, Nyman M, Saarela M, Watzl B (2015) Contribution of diet to the composition of the human gut microbiota. Microb Ecol Health Dis 26:26164. doi:10.3402/mehd.v26.26164 PubMedGoogle Scholar
  27. Ho CS, Lam CW, Chan MH, Cheung RC, Law LK, Lit LC, Ng KF, Suen MW, Tai HL (2003) Electrospray ionisation mass spectrometry: principles and clinical applications. Clin Biochem Rev 24(1):3–12PubMedPubMedCentralGoogle Scholar
  28. Human Microbiome Jumpstart Reference Strains C, Nelson KE, Weinstock GM, Highlander SK, Worley KC, Creasy HH, Wortman JR, Rusch DB, Mitreva M, Sodergren E, Chinwalla AT, Feldgarden M, Gevers D, Haas BJ, Madupu R, Ward DV, Birren BW, Gibbs RA, Methe B, Petrosino JF, Strausberg RL, Sutton GG, White OR, Wilson RK, Durkin S, Giglio MG, Gujja S, Howarth C, Kodira CD, Kyrpides N, Mehta T, Muzny DM, Pearson M, Pepin K, Pati A, Qin X, Yandava C, Zeng Q, Zhang L, Berlin AM, Chen L, Hepburn TA, Johnson J, McCorrison J, Miller J, Minx P, Nusbaum C, Russ C, Sykes SM, Tomlinson CM, Young S, Warren WC, Badger J, Crabtree J, Markowitz VM, Orvis J, Cree A, Ferriera S, Fulton LL, Fulton RS, Gillis M, Hemphill LD, Joshi V, Kovar C, Torralba M, Wetterstrand KA, Abouellleil A, Wollam AM, Buhay CJ, Ding Y, Dugan S, FitzGerald MG, Holder M, Hostetler J, Clifton SW, Allen-Vercoe E, Earl AM, Farmer CN, Liolios K, Surette MG, Xu Q, Pohl C, Wilczek-Boney K, Zhu D (2010) A catalog of reference genomes from the human microbiome. Science 328(5981):994–999. doi:10.1126/science.1183605 CrossRefGoogle Scholar
  29. Human Microbiome Project C (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214. doi:10.1038/nature11234 CrossRefGoogle Scholar
  30. Iraporda C, Errea A, Romanin DE, Cayet D, Pereyra E, Pignataro O, Sirard JC, Garrote GL, Abraham AG, Rumbo M (2015) Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology 220(10):1161–1169. doi:10.1016/j.imbio.2015.06.004 CrossRefPubMedGoogle Scholar
  31. Jansen R, Lachatre G, Marquet P (2005) LC-MS/MS systematic toxicological analysis: comparison of MS/MS spectra obtained with different instruments and settings. Clin Biochem 38(4):362–372. doi:10.1016/j.clinbiochem.2004.11.003 CrossRefPubMedGoogle Scholar
  32. Kane AV, Dinh DM, Ward HD (2015) Childhood malnutrition and the intestinal microbiome. Pediatr Res 77(1–2):256–262. doi:10.1038/pr.2014.179 CrossRefPubMedGoogle Scholar
  33. Karlsson F, Tremaroli V, Nielsen J, Backhed F (2013) Assessing the human gut microbiota in metabolic diseases. Diabetes 62(10):3341–3349. doi:10.2337/db13-0844 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kasparovska J, Pecinkova M, Dadakova K, Krizova L, Hadrova S, Lexa M, Lochman J, Kasparovsky T (2016) Effects of isoflavone-enriched feed on the rumen microbiota in dairy cows. PLoS One 11(4):e0154642. doi:10.1371/journal.pone.0154642 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kawashima Y, Takahashi N, Satoh M, Saito T, Kado S, Nomura F, Matsumoto H, Kodera Y (2013) Enhanced recovery of lyophilized peptides in shotgun proteomics by using an LC-ESI-MS compatible surfactant. Proteomics 13(5):751–755. doi:10.1002/pmic.201200462 CrossRefPubMedGoogle Scholar
  36. Klaassens ES, de Vos WM, Vaughan EE (2007) Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract. Appl Environ Microbiol 73(4):1388–1392. doi:10.1128/AEM.01921-06 CrossRefPubMedGoogle Scholar
  37. Kolmeder CA, de Vos WM (2014) Metaproteomics of our microbiome—developing insight in function and activity in man and model systems. J Proteome 97:3–16. doi:10.1016/j.jprot.2013.05.018 CrossRefGoogle Scholar
  38. Kolmeder CA, de Been M, Nikkilä J, Ritamo I, Mättö J, Valmu L, Salojärvi J, Palva A, Salonen A, de Vos WM (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. doi:10.1371/journal.pone.0029913 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lazarou J, Pomeranz BH, Corey PN (1998) Incidence of adverse drug reactions in hospitalized patients: a meta-analysis of prospective studies. JAMA 279(15):1200–1205CrossRefPubMedGoogle Scholar
  40. Leary DH, Hervey WJ, Li RW, Deschamps JR, Kusterbeck AW, Vora GJ (2012) Method development for metaproteomic analyses of marine biofilms. Anal Chem 84(9):4006–4013. doi:10.1021/ac203315n CrossRefPubMedGoogle Scholar
  41. Levi Mortera S, Del Chierico F, Vernocchi P, Rosado MM, Cavola A, Chierici M, Pieroni L, Urbani A, Carsetti R, Lante I, Dallapiccola B, Putignani L (2016) Monitoring perinatal gut microbiota in mouse models by mass spectrometry approaches: parental genetic background and breastfeeding effects. Front Microbiol 7:1523. doi:10.3389/fmicb.2016.01523 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124(4):837–848. doi:10.1016/j.cell.2006.02.017 CrossRefPubMedGoogle Scholar
  43. Lipecka J, Chhuon C, Bourderioux M, Bessard MA, van Endert P, Edelman A, Guerrera IC (2016) Sensitivity of mass spectrometry analysis depends on the shape of the filtration unit used for filter aided sample preparation (FASP). Proteomics 16(13):1852–1857. doi:10.1002/pmic.201600103 CrossRefPubMedGoogle Scholar
  44. Lopez JL, Marina A, Alvarez G, Vazquez J (2002) Application of proteomics for fast identification of species-specific peptides from marine species. Proteomics 2(12):1658–1665. doi:10.1002/1615-9861(200212)2:12<1658::AID-PROT1658>3.0.CO;2-4 CrossRefPubMedGoogle Scholar
  45. Maeda Y, Kumanogoh A, Takeda K (2016) Altered composition of gut microbiota in rheumatoid arthritis patients. Nihon Rinsho Meneki Gakkai Kaishi 39(1):59–63. doi:10.2177/jsci.39.59 CrossRefPubMedGoogle Scholar
  46. Magrone T, Jirillo E (2013) The interaction between gut microbiota and age-related changes in immune function and inflammation. Immun Ageing 10(1):31. doi:10.1186/1742-4933-10-31 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Malaguarnera G, Giordano M, Nunnari G, Bertino G, Malaguarnera M (2014) Gut microbiota in alcoholic liver disease: pathogenetic role and therapeutic perspectives. World J Gastroenterol 20(44):16639–16648. doi:10.3748/wjg.v20.i44.16639 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mangiola F, Ianiro G, Franceschi F, Fagiuoli S, Gasbarrini G, Gasbarrini A (2016) Gut microbiota in autism and mood disorders. World J Gastroenterol 22(1):361–368. doi:10.3748/wjg.v22.i1.361 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Martin C, Zhang Y, Tonelli C, Petroni K (2013) Plants, diet, and health. Annu Rev Plant Biol 64:19–46. doi:10.1146/annurev-arplant-050312-120142 CrossRefPubMedGoogle Scholar
  50. Mawuenyega KG, Kaji H, Yamuchi Y, Shinkawa T, Saito H, Taoka M, Takahashi N, Isobe T (2003) Large-scale identification of Caenorhabditis elegans proteins by multidimensional liquid chromatography-tandem mass spectrometry. J Proteome Res 2(1):23–35CrossRefPubMedGoogle Scholar
  51. Mayne J, Ning Z, Zhang X, Starr AE, Chen R, Deeke S, Chiang CK, Xu B, Wen M, Cheng K, Seebun D, Star A, Moore JI, Figeys D (2016) Bottom-up proteomics (2013-2015): keeping up in the era of systems biology. Anal Chem 88(1):95–121. doi:10.1021/acs.analchem.5b04230 CrossRefPubMedGoogle Scholar
  52. Muth T, Benndorf D, Reichl U, Rapp E, Martens L (2013) Searching for a needle in a stack of needles: challenges in metaproteomics data analysis. Mol BioSyst 9(4):578–585. doi:10.1039/c2mb25415h CrossRefPubMedGoogle Scholar
  53. Nesvizhskii AI, Aebersold R (2005) Interpretation of shotgun proteomic data: the protein inference problem. Mol Cell Proteomics 4(10):1419–1440. doi:10.1074/mcp.R500012-MCP200 CrossRefPubMedGoogle Scholar
  54. Noordin R, Othman N (2013) Proteomics technology—a powerful tool for the biomedical scientists. Malays J Med Sci 20(2):1–2PubMedPubMedCentralGoogle Scholar
  55. Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao JZ, Abe F, Osawa R (2016) Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol 16:90. doi:10.1186/s12866-016-0708-5 CrossRefPubMedPubMedCentralGoogle Scholar
  56. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250(10):4007–4021PubMedPubMedCentralGoogle Scholar
  57. O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7(7):688–693. doi:10.1038/sj.embor.7400731 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Peach M, Marsh N, Miskiewicz EI, MacPhee DJ (2015) Solubilization of proteins: the importance of lysis buffer choice. Methods Mol Biol 1312:49–60. doi:10.1007/978-1-4939-2694-7_8 CrossRefPubMedGoogle Scholar
  59. Perez-Cobas AE, Gosalbes MJ, Friedrichs A, Knecht H, Artacho A, Eismann K, Otto W, Rojo D, Bargiela R, von Bergen M, Neulinger SC, Däumer C, Heinsen FA, Latorre A, Barbas C, Seifert J, dos Santos VM, Ott SJ, Ferrer M, Moya A (2013) Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut 62(11):1591–1601. doi:10.1136/gutjnl-2012-303184 CrossRefPubMedGoogle Scholar
  60. Pinter M, Trauner M, Peck-Radosavljevic M, Sieghart W (2016) Cancer and liver cirrhosis: implications on prognosis and management. ESMO Open 1(2):e000042. doi:10.1136/esmoopen-2016-000042 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Prauchner CA, Kozloski GV, Farenzena R (2013) Evaluation of sonication treatment and buffer composition on rumen bacteria protein extraction and carboxymethylcellulase activity. J Sci Food Agric 93(7):1733–1736. doi:10.1002/jsfa.5959 CrossRefPubMedGoogle Scholar
  62. Quan Q, Szeto SS, Law HC, Zhang Z, Wang Y, Chu IK (2015) Fully automated multidimensional reversed-phase liquid chromatography with tandem anion/cation exchange columns for simultaneous global endogenous tyrosine nitration detection, integral membrane protein characterization, and quantitative proteomics mapping in cerebral infarcts. Anal Chem 87(19):10015–10024. doi:10.1021/acs.analchem.5b02619 CrossRefPubMedGoogle Scholar
  63. Redon E, Loubiere P, Cocaign-Bousquet M (2005) Role of mRNA stability during genome-wide adaptation of Lactococcus lactis to carbon starvation. J Biol Chem 280(43):36380–36385. doi:10.1074/jbc.M506006200 CrossRefPubMedGoogle Scholar
  64. Rose C, Parker A, Jefferson B, Cartmell E (2015) The characterization of feces and urine: a review of the literature to inform advanced treatment technology. Crit Rev Environ Sci Technol 45(17):1827–1879. doi:10.1080/10643389.2014.1000761 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Satija A, Bhupathiraju SN, Rimm EB, Spiegelman D, Chiuve SE, Borgi L, Willett WC, Manson JE, Sun Q, Hu FB (2016) Plant-based dietary patterns and incidence of type 2 diabetes in US men and women: results from three prospective cohort studies. PLoS Med 13(6):e1002039. doi:10.1371/journal.pmed.1002039 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6(9):1749–1762. doi:10.1038/ismej.2012.11 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Slebos RJ, Brock JW, Winters NF, Stuart SR, Martinez MA, Li M, Chambers MC, Zimmerman LJ, Ham AJ, Tabb DL, Liebler DC (2008) Evaluation of strong cation exchange versus isoelectric focusing of peptides for multidimensional liquid chromatography-tandem mass spectrometry. J Proteome Res 7(12):5286–5294. doi:10.1021/pr8004666 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Soltwisch J, Souady J, Berkenkamp S, Dreisewerd K (2009) Effect of gas pressure and gas type on the fragmentation of peptide and oligosaccharide ions generated in an elevated pressure UV/IR-MALDI ion source coupled to an orthogonal time-of-flight mass spectrometer. Anal Chem 81(8):2921–2934. doi:10.1021/ac802301s CrossRefPubMedGoogle Scholar
  69. Sonnenburg JL, Backhed F (2016) Diet-microbiota interactions as moderators of human metabolism. Nature 535(7610):56–64. doi:10.1038/nature18846 CrossRefPubMedGoogle Scholar
  70. Stephen AM, Cummings JH (1980) The microbial contribution to human faecal mass. J Med Microbiol 13(1):45–56. doi:10.1099/00222615-13-1-45 CrossRefPubMedGoogle Scholar
  71. Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299(6710):1259–1260CrossRefPubMedPubMedCentralGoogle Scholar
  72. Strati F, Di Paola M, Stefanini I, Albanese D, Rizzetto L, Lionetti P, Calabrò A, Jousson O, Donati C, Cavalieri D, De Filippo C (2016) Age and gender affect the composition of fungal population of the human gastrointestinal tract. Front Microbiol 7:1227. doi:10.3389/fmicb.2016.01227 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Tai N, Wong FS, Wen L (2015) The role of gut microbiota in the development of type 1, type 2 diabetes mellitus and obesity. Rev Endocr Metab Disord 16(1):55–65. doi:10.1007/s11154-015-9309-0 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Tanca A, Palomba A, Pisanu S, Addis MF, Uzzau S (2015) Enrichment or depletion? The impact of stool pretreatment on metaproteomic characterization of the human gut microbiota. Proteomics 15(20):3474–3485. doi:10.1002/pmic.201400573 CrossRefPubMedGoogle Scholar
  75. Tang Y, Underwood A, Gielbert A, Woodward MJ, Petrovska L (2014) Metaproteomics analysis reveals the adaptation process for the chicken gut microbiota. Appl Environ Microbiol 80(2):478–485. doi:10.1128/AEM.02472-13 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Tlaskalová-Hogenová H, Stěpánková R, Kozáková H, Hudcovic T, Vannucci L, Tučková L, Rossmann P, Hrnčíř T, Kverka M, Zákostelská Z, Klimešová K, Přibylová J, Bártová J, Sanchez D, Fundová P, Borovská D, Srůtková D, Zídek Z, Schwarzer M, Drastich P, Funda DP (2011) The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol 8(2):110–120. doi:10.1038/cmi.2010.67 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Trufelli H, Palma P, Famiglini G, Cappiello A (2011) An overview of matrix effects in liquid chromatography-mass spectrometry. Mass Spectrom Rev 30(3):491–509. doi:10.1002/mas.20298 CrossRefPubMedGoogle Scholar
  78. Verberkmoes NC, Russell AL, Shah M, Godzik A, Rosenquist M, Halfvarson J, Lefsrud MG, Apajalahti J, Tysk C, Hettich RL, Jansson JK (2009) Shotgun metaproteomics of the human distal gut microbiota. ISME J 3(2):179–189. doi:10.1038/ismej.2008.108 CrossRefPubMedGoogle Scholar
  79. Vernocchi P, Del Chierico F, Putignani L (2016) Gut microbiota profiling: metabolomics based approach to unravel compounds affecting human health. Front Microbiol 7:1144. doi:10.3389/fmicb.2016.01144 CrossRefPubMedPubMedCentralGoogle Scholar
  80. von Mutius E (2010) 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: farm lifestyles and the hygiene hypothesis. Clin Exp Immunol 160(1):130–135. doi:10.1111/j.1365-2249.2010.04138.x CrossRefGoogle Scholar
  81. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63. doi:10.1038/nrg2484 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wang HB, Zhang ZX, Li H, He HB, Fang CX, Zhang AJ, Li QS, Chen RS, Guo XK, Lin HF, Wu LK, Lin S, Chen T, Lin RY, Peng XX, Lin WX (2011) Characterization of metaproteomics in crop rhizospheric soil. J Proteome Res 10(3):932–940. doi:10.1021/pr100981r CrossRefPubMedGoogle Scholar
  83. Wang J, Cunningham R, Zetterberg H, Asthana S, Carlsson C, Okonkwo O, Li L (2016) Label-free quantitative comparison of cerebrospinal fluid glycoproteins and endogenous peptides in subjects with Alzheimer’s disease, mild cognitive impairment and healthy individuals. Proteomics Clin Appl 10(12):1225–1241. doi:10.1002/prca.201600009 CrossRefPubMedGoogle Scholar
  84. 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 Gastroenterol 16(1):121. doi:10.1186/s12876-016-0534-0 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Westergaard D, Li J, Jensen K, Kouskoumvekaki I, Panagiotou G (2014) Exploring mechanisms of diet-colon cancer associations through candidate molecular interaction networks. BMC Genomics 15:380. doi:10.1186/1471-2164-15-380 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Whitehouse CM, Dreyer RN, Yamashita M, Fenn JB (1985) Electrospray interface for liquid chromatographs and mass spectrometers. Anal Chem 57(3):675–679CrossRefPubMedGoogle Scholar
  87. Wilmes P, Bond PL (2004) The application of two-dimensional polyacrylamide gel electrophoresis and downstream analyses to a mixed community of prokaryotic microorganisms. Environ Microbiol 6(9):911–920. doi:10.1111/j.1462-2920.2004.00687.x CrossRefPubMedGoogle Scholar
  88. Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6(5):359–362. doi:10.1038/nmeth.1322 CrossRefPubMedGoogle Scholar
  89. Wong K, Shaw TI, Oladeinde A, Glenn TC, Oakley B, Molina M (2016) Rapid microbiome changes in freshly deposited cow feces under field conditions. Front Microbiol 7:500. doi:10.3389/fmicb.2016.00500 PubMedPubMedCentralGoogle Scholar
  90. Xie H, Guo R, Zhong H, Feng Q, Lan Z, Qin B, Ward KJ, Jackson MA, Xia Y, Chen X, Chen B, Xia H, Xu C, Li F, Xu X, Al-Aama JY, Yang H, Wang J, Kristiansen K, Wang J, Steves CJ, Bell JT, Li J, Spector TD, Jia H (2016) Shotgun metagenomics of 250 adult twins reveals genetic and environmental impacts on the gut microbiome. Cell Syst 3(6):572–584. doi:10.1016/j.cels.2016.10.004 CrossRefPubMedGoogle Scholar
  91. Xiong W, Giannone RJ, Morowitz MJ, Banfield JF, Hettich RL (2015) Development of an enhanced metaproteomic approach for deepening the microbiome characterization of the human infant gut. J Proteome Res 14(1):133–141. doi:10.1021/pr500936p CrossRefPubMedGoogle Scholar
  92. Xu X, Shi L, Wang M (2016) Comparative quantitative proteomics unveils putative mechanisms involved into mercury toxicity and tolerance in Tigriopus japonicus under multigenerational exposure scenario. Environ Pollut 218:1287–1297. doi:10.1016/j.envpol.2016.08.087 CrossRefPubMedGoogle Scholar
  93. Zhang M, Yang XJ (2016) Effects of a high fat diet on intestinal microbiota and gastrointestinal diseases. World J Gastroenterol 22(40):8905–8909. doi:10.3748/wjg.v22.i40.8905 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Zhang W, Zhong T, Chen Y (2016a) LC-MS/MS-based targeted proteomics quantitatively detects the interaction between p53 and MDM2 in breast cancer. J Proteome 152:172–180. doi:10.1016/j.jprot.2016.11.002 CrossRefGoogle Scholar
  95. Zhang X, Hou HT, Wang J, Liu XC, Yang Q, He GW (2016b) Plasma proteomic study in pulmonary arterial hypertension associated with congenital heart diseases. Sci Rep 6:36541. doi:10.1038/srep36541 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Zhang X, Ning Z, Mayne J, Moore JI, Li J, Butcher J, Deeke SA, Chen R, Chiang CK, Wen M, Mack D, Stintzi A, Figeys D (2016c) MetaPro-IQ: a universal metaproteomic approach to studying human and mouse gut microbiota. Microbiome 4(1):31. doi:10.1186/s40168-016-0176-z CrossRefPubMedPubMedCentralGoogle Scholar
  97. Zhao X, Jiang Z, Yang F, Wang Y, Gao X, Wang Y, Chai X, Pan G, Zhu Y (2016) Sensitive and simplified detection of antibiotic influence on the dynamic and versatile changes of fecal short-chain fatty acids. PLoS One 11(12):e0167032. doi:10.1371/journal.pone.0167032 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Zhou Y, Meng Z, Edman-Woolcott M, Hamm-Alvarez SF, Zandi E (2015) Multidimensional separation using HILIC and SCX pre-fractionation for RP LC-MS/MS platform with automated exclusion list-based MS data acquisition with increased protein quantification. J Proteomics Bioinform 8(11):260–265. doi:10.4172/jpb.1000378 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Zhu W, Gregory JC, Org E, Buffa JA, Gupta N, Wang Z, Li L, Fu X, Wu Y, Mehrabian M, Sartor RB, McIntyre TM, Silverstein RL, Tang WH, DiDonato JA, Brown JM, Lusis AJ, Hazen SL (2016) Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell 165(1):111–124. doi:10.1016/j.cell.2016.02.011 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Mingming Xiao
    • 1
    • 2
  • Junjun Yang
    • 1
    • 2
  • Yuxin Feng
    • 1
    • 2
  • Yan Zhu
    • 1
    • 2
  • Xin Chai
    • 1
    • 2
  • Yuefei Wang
    • 1
    • 2
  1. 1.Tianjin State Key Laboratory of Modern Chinese MedicineTianjin University of Traditional Chinese MedicineTianjinChina
  2. 2.Research and Development Center of Traditional Chinese MedicineTianjin International Joint Academy of Biotechnology and MedicineTianjinChina

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