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Protective role of gut commensal microbes against intestinal infections

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An Erratum to this article was published on 04 January 2015

Abstract

The human gastrointestinal tract is colonized by multitudes of microorganisms that exert beneficial effects on human health. Mounting evidence suggests that intestinal microbiota contributes to host resistance against enteropathogenic bacterial infection. However, molecular details that account for such an important role has just begun to be understood. The commensal microbes in the intestine regulate gut homeostasis through activating the development of host innate immunity and producing molecules with antimicrobial activities that directly inhibit propagation of pathogenic bacteria. Understanding the protective roles of gut microbiota will provide a better insight into the molecular basis that underlies complicated interaction among host-pathogen-symbiont. In this review, we highlighted recent findings that help us broaden our knowledge of the intestinal ecosystem and thereby come up with a better strategy for combating enteropathogenic infection.

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References

  • Backhed, F., Ley, R.E., Sonnenburg, J.L., Peterson, D.A., and Gordon, J.I. 2005. Host-bacterial mutualism in the human intestine. Science 307, 1915–1920.

    Article  PubMed  Google Scholar 

  • Bari, W., Lee, K.M., and Yoon, S.S. 2012. Structural and functional importance of outer membrane proteins in Vibrio cholerae flagellum. J. Microbiol. 50, 631–637.

    Article  PubMed  Google Scholar 

  • Bassler, B.L. 1999. How bacteria talk to each other: Regulation of gene expression by quorum sensing. Curr. Opin. Microbiol. 2, 582–587.

    Article  CAS  PubMed  Google Scholar 

  • Brown, E.M., Sadarangani, M., and Finlay, B.B. 2013. The role of the immune system in governing host-microbe interactions in the intestine. Nat. Immunol. 14, 660–667.

    Article  CAS  PubMed  Google Scholar 

  • Buffie, C.G. and Pamer, E.G. 2013. Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13, 790–801.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cash, H.L., Whitham, C.V., Behrendt, C.L., and Hooper, L.V. 2006. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126–1130.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cerf-Bensussan, N. and Gaboriau-Routhiau, V. 2010. The immune system and the gut microbiota: friends or foes? Nat. Rev. Immunol. 10, 735–744.

    Article  CAS  PubMed  Google Scholar 

  • Clarke, M.B., Hughes, D.T., Zhu, C., Boedeker, E.C., and Sperandio, V. 2006. The QseC sensor kinase: A bacterial adrenergic receptor. Proc. Natl. Acad. Sci. USA 103, 10420–10425.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clemente, J.C., Ursell, L.K., Parfrey, L.W., and Knight, R. 2012. The impact of the gut microbiota on human health: An integrative view. Cell 148, 1258–1270.

    Article  CAS  PubMed  Google Scholar 

  • Collins, J.W., Keeney, K.M., Crepin, V.F., Rathinam, V.A.K., Fitzgerald, K.A., Finlay, B.B., and Frankel, G. 2014. Citrobacter rodentium: Infection, inflammation and the microbiota. Nat. Rev. Microbiol. 12, 612–623.

    Article  CAS  PubMed  Google Scholar 

  • Conte, M.P., Schippa, S., Zamboni, I., Penta, M., Chiarini, F., Seganti, L., Osborn, J., Falconieri, P., Borrelli, O., and Cucchiara, S. 2006. Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut 55, 1760–1767.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Corr, S.C., Gahan, C.G., and Hill, C. 2007. Impact of selected Lactobacillus and Bifidobacterium species on Listeria monocytogenes infection and the mucosal immune response. FEMS Immunol. Med. Microbiol. 50, 380–388.

    Article  CAS  PubMed  Google Scholar 

  • Crost, E.H., Ajandouz, E.H., Villard, C., Geraert, P.A., Puigserver, A., and Fons, M. 2011. Ruminococcin C, a new anti-Clostridium perfringens bacteriocin produced in the gut by the commensal bacterium Ruminococcus gnavus E1. Biochimie 93, 1487–1494.

    Article  CAS  PubMed  Google Scholar 

  • Dong, Y.H., Xu, J.L., Li, X.Z., and Zhang, L.H. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 97, 3526–3531.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eckburg, P., Bik, E., Bernstein, C., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S., Nelson, K., and Relman, D. 2005. Diversity of the human intestinal microbial flora. Science 308, 1635–1638.

    Article  PubMed Central  PubMed  Google Scholar 

  • Endt, K., Stecher, B., Chaffron, S., Slack, E., Tchitchek, N., Benecke, A., Van Maele, L., Sirard, J.C., Mueller, A.J., Heikenwalder, M., and et al. 2010. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog. 6, e1001097.

    Article  Google Scholar 

  • Ferreira, R.B.R., Gill, N., Willing, B.P., Antunes, L.C.M., Russell, S.L., Croxen, M.A., and Finlay, B.B. 2011. The intestinal microbiota plays a role in Salmonella-induced colitis independent of pathogen colonization. PLoS One 6, e20338.

    Article  Google Scholar 

  • Fujimura, K.E., Slusher, N.A., Cabana, M.D., and Lynch, S.V. 2010. Role of the gut microbiota in defining human health. Expert Rev. Anti-infective Ther. 8, 435–454.

    Article  Google Scholar 

  • Fukuda, S., Toh, H., Hase, K., Oshima, K., Nakanishi, Y., Yoshimura, K., Tobe, T., Clarke, J.M., Topping, D.L., Suzuki, T., and et al. 2011. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543–547.

    Article  CAS  PubMed  Google Scholar 

  • Gareau, M.G., Sherman, P.M., and Walker, W.A. 2010. Probiotics and the gut microbiota in intestinal health and disease. Nat. Rev. Gastroenterol Hepatol. 7, 503–514.

    Article  PubMed  Google Scholar 

  • Garland, C., Lee, A., and Dickson, M. 1982. Segmented filamentous bacteria in the rodent small intestine: Their colonization of growing animals and possible role in host resistance to Salmonella. Microb. Ecol. 8, 181–190.

    Article  CAS  PubMed  Google Scholar 

  • Gomez, A., Ladiré, M., Marcille, F., and Fons, M. 2002. Trypsin mediates growth phase-dependent transcriptional regulation of genes involved in biosynthesis of ruminococcin A, a lantibiotic produced by a Ruminococcus gnavus strain from a human intestinal microbiota. J. Bacteriol. 184, 18–28.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guarner, F. and Malagelada, J.R. 2003. Gut flora in health and disease. Lancet 361, 512–519.

    Article  PubMed  Google Scholar 

  • He, F., Ouwehan, A.C., Hashimoto, H., Isolauri, E., Benno, Y., and Salminen, S. 2001. Adhesion of Bifidobacterium spp. to human intestinal mucus. Microbiol. Immunol. 45, 259–262.

    Article  CAS  PubMed  Google Scholar 

  • Hooper, L.V., Littman, D.R., and Macpherson, A.J. 2012. Interactions between the microbiota and the immune system. Science 336, 1268–1273.

    Article  CAS  PubMed  Google Scholar 

  • Hsiao, A., Ahmed, A.M.S., Subramanian, S., Griffin, N.W., Drewry, L.L., Petri, W.A., Haque, R., Ahmed, T., and Gordon, J.I. 2014. Members of the human gut microbiota involved in recovery from Vibrio cholerae infection. Nature. doi: 10.1038/nature13738.

    Google Scholar 

  • Ismail, A. and Hooper, L. 2005. Epithelial cells and their neighbors. Iv. Bacterial contributions to intestinal epithelial barrier integrity. Am. J. Physiol. Gastrointest Liver Physiol. 289, G779–G784.

    Article  CAS  PubMed  Google Scholar 

  • Isolauri, E. 2003. Probiotics for infectious diarrhoea. Gut 52, 436–437.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jacobi, C., Grundler, S., Hsieh, C.J., Frick, J.S., Adam, P., Lamprecht, G., Autenrieth, I., Gregor, M., and Malfertheiner, P. 2012. Quorum sensing in the probiotic bacterium Escherichia coli Nissle 1917 (Mutaflor) — evidence that furanosyl borate diester (Ai-2) is influencing the cytokine expression in the DSS colitis mouse model. Gut Pathog. 4, 8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johansson, M.E.V., Phillipson, M., Petersson, J., Velcich, A., Holm, L., and Hansson, G.C. 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. USA 105, 15064–15069.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kamada, N., Chen, G.Y., Inohara, N., and Nunez, G. 2013. Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14, 685–690.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kamada, N., Kim, Y.G., Sham, H.P., Vallance, B.A., Puente, J.L., Martens, E.C., and Núñez, G. 2012. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336, 1325–1329.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Karczewski, J., Troost, F.J., Konings, I., Dekker, J., Kleerebezem, M., Brummer, R.J., and Wells, J.M. 2010. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am. J. Physiol. Gastrointest Liver Physiol. 298, G851–859.

    Article  Google Scholar 

  • Kelly, D., Campbell, J.I., King, T.P., Grant, G., Jansson, E.A., Coutts, A.G., Pettersson, S., and Conway, S. 2004. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat. Immunol. 5, 104–112.

    Article  CAS  PubMed  Google Scholar 

  • Khachatryan, Z.A., Ktsoyan, Z.A., Manukyan, G.P., Kelly, D., Ghazaryan, K.A., and Aminov, R.I. 2008. Predominant role of host genetics in controlling the composition of gut microbiota. PLoS One 3, e3064.

    Article  Google Scholar 

  • Kim, J.E., Kim, M.S., Yoon, Y.S., Chung, M.J., and Yum, D.Y. 2014. Use of selected lactic acid bacteria in the eradication of Helicobacter pylori infection. J. Microbiol. 52, 955–962.

    Article  CAS  PubMed  Google Scholar 

  • Kwon, A.S., Lim, D.H., Shin, H.J., Park, G., Reu, J.H., Park, H.J., Kim, J., and Lim, Y. 2013. The N3 subdomain in a domain of fibronectin-binding protein B isotype I is an independent risk determinant predictive for biofilm formation of Staphylococcus aureus clinical isolates. J. Microbiol. 51, 499–505.

    Article  CAS  PubMed  Google Scholar 

  • Lee, K.M., Yoon, M.Y., Park, Y., Lee, J.H., and Yoon, S.S. 2011. Anaerobiosis-induced loss of cytotoxicity is due to inactivation of quorum sensing in Pseudomonas aeruginosa. Infect. Immun. 79, 2792–2800.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lievin-Le Moal, V., Amsellem, R., Servin, A.L., and Coconnier, M.H. 2002. Lactobacillus acidophilus (strain LB) from the resident adult human gastrointestinal microflora exerts activity against brush border damage promoted by a diarrhoeagenic Escherichia coli in human enterocyte-like cells. Gut 50, 803–811.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lopez-Boado, Y.S., Wilson, C.L., Hooper, L.V., Gordon, J.I., Hultgren, S.J., and Parks, W.C. 2000. Bacterial exposure induces and activates matrilysin in mucosal epithelial cells. J. Cell Biol. 148, 1305–1315.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mack, D.R., Michail, S., Wei, S., McDougall, L., and Hollingsworth, M.A. 1999. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am. J. Physiol. 276, G941–950.

    Google Scholar 

  • Makras, L. and De Vuyst, L. 2006. The in vitro inhibition of Gram-negative pathogenic bacteria by bifidobacteria is caused by the production of organic acids. Intl. Dairy J. 16, 1049–1057.

    Article  CAS  Google Scholar 

  • Marcille, F., Gomez, A., Joubert, P., Ladiré, M., Veau, G., Clara, A., Gavini, F., Willems, A., and Fons, M. 2002. Distribution of genes encoding the trypsin-dependent lantibiotic ruminococcin a among bacteria isolated from human fecal microbiota. Appl. Environ. Microbiol. 68, 3424–3431.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maslowski, K.M., Vieira, A.T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H.C., Rolph, M.S., Mackay, F., Artis, D., and et al. 2009. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461, 1282–1286.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Medellin-Peña, M.J. and Griffiths, M.W. 2009. Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Appl. Environ. Microbiol. 75, 1165–1172.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mundy, R., MacDonald, T.T., Dougan, G., Frankel, G., and Wiles, S. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7, 1697–1706.

    Article  CAS  PubMed  Google Scholar 

  • Nava, G.M. and Stappenbeck, T.S. 2011. Diversity of the autochthonous colonic microbiota. Gut Microbes 2, 99–104.

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Hara, A.M. and Shanahan, F. 2007. Gut microbiota: Mining for therapeutic potential. Clin. Gastroenterol. Hepatol. 5, 274–284.

    Article  PubMed  Google Scholar 

  • Petnicki-Ocwieja, T., Hrncir, T., Liu, Y.J., Biswas, A., Hudcovic, T., Tlaskalova-Hogenova, H., and Kobayashi, K.S. 2009. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc. Natl. Acad. Sci. USA 106, 15813–15818.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Philpott, D. and Girardin, S. 2004. The role of toll-like receptors and nod proteins in bacterial infection. Mol. Immunol. 41, 1099–1108.

    Article  CAS  PubMed  Google Scholar 

  • Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., and et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rea, M.C., Sit, C.S., Clayton, E., O’Connor, P.M., Whittal, R.M., Zheng, J., Vederas, J.C., Ross, R.P., and Hill, C. 2010. Thuricin Cd, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc. Natl. Acad. Sci. USA 107, 9352–9357.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sekirov, I., Russell, S.L., Antunes, L.C.M., and Finlay, B.B. 2010. Gut microbiota in health and disease. Physiol. Rev. 90, 859–904.

    Article  CAS  PubMed  Google Scholar 

  • Seong, W.J., Kwon, H.J., Kim, T.E., Lee, D.Y., Park, M.S., and Kim, J.H. 2012. Molecular serotyping of Salmonella enterica by complete rpoB gene sequencing. J. Microbiol. 50, 962–969.

    Article  CAS  PubMed  Google Scholar 

  • Shanahan, F. 2002. The host-microbe interface within the gut. Best Pract. Res. Clin. Gastroenterol. 16, 915–931.

    Article  PubMed  Google Scholar 

  • Sonnenburg, J.L., Xu, J., Leip, D.D., Chen, C.H., Westover, B.P., Weatherford, J., Buhler, J.D., and Gordon, J.I. 2005. Glycan for-aging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955–1959.

    Article  CAS  PubMed  Google Scholar 

  • Sperandio, V. 2010. SdiA sensing of acyl-homoserine lactones by enterohemorrhagic E. coli (EHEC) serotype O157:H7 in the bovine rumen. Gut Microbes 1, 432–435.

    Article  PubMed Central  PubMed  Google Scholar 

  • Sperandio, V., Torres, A.G., Jarvis, B., Nataro, J.P., and Kaper, J.B. 2003. Bacteria-host communication: The language of hormones. Proc. Natl. Acad. Sci. USA 100, 8951–8956.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Synnott, A., Ohshima, K., Nakai, Y., and Tanji, Y. 2009. IgA response of BALB/c mice to orally administered Salmonella typhimurium flagellin-displaying T2 bacteriophages. Biotechnol. Prog. 25, 552–558.

    Article  CAS  PubMed  Google Scholar 

  • Tanoue, T., Umesaki, Y., and Honda, K. 2010. Immune responses to gut microbiota-commensals and pathogens. Gut Microbes 1, 224–233.

    Article  PubMed Central  PubMed  Google Scholar 

  • Tsai, P.W., Cheng, Y.L., Hsieh, W.P., and Lan, C.Y. 2014. Responses of Candida albicans to the human antimicrobial peptide ll-37. J. Microbiol. 52, 581–589.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, C.L., Ouellette, A.J., Satchell, D.P., Ayabe, T., López-Boado, Y.S., Stratman, J.L., Hultgren, S.J., Matrisian, L.M., and Parks, W.C. 1999. Regulation of intestinal α-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286, 113–117.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y.X., Xu, Z.H., Zhang, Y.Q., Tian, J., Weng, L.X., and Wang, L.H. 2012. A new quorum-sensing inhibitor attenuates virulence and decreases antibiotic resistance in Pseudomonas aeruginosa. J. Microbiol. 50, 987–993.

    Article  CAS  PubMed  Google Scholar 

  • Yoon, M.Y., Lee, K.M., Yoon, Y., Go, J., Park, Y., Cho, Y.J., Tannock, G.W., and Yoon, S.S. 2013. Functional screening of a metagenomic library reveals operons responsible for enhanced intestinal colonization by gut commensal microbes. Appl. Environ. Microbiol. 79, 3829–3838.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao, Z.G., Yan, S.S., Yu, Y.M., Mi, N., Zhang, L.X., Liu, J., Li, X.L., Liu, F., Xu, J.F., Yang, W.Q., and Li, G.M. 2013. An aqueous extract of Yunnan Baiyao inhibits the quorum-sensing-related virulence of Pseudomonas aeruginosa. J. Microbiol. 51, 207–212.

    Article  CAS  PubMed  Google Scholar 

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Yoon, M.Y., Lee, K. & Yoon, S.S. Protective role of gut commensal microbes against intestinal infections. J Microbiol. 52, 983–989 (2014). https://doi.org/10.1007/s12275-014-4655-2

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