Advertisement

Journal of Microbiology

, Volume 52, Issue 12, pp 983–989 | Cite as

Protective role of gut commensal microbes against intestinal infections

  • My Young Yoon
  • Keehoon Lee
  • Sang Sun YoonEmail author
Minireview
First Online:

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.

Keywords

gut microbiota enteropathogenic bacterial infection colonization resistance 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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.PubMedCrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. Bassler, B.L. 1999. How bacteria talk to each other: Regulation of gene expression by quorum sensing. Curr. Opin. Microbiol. 2, 582–587.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. Buffie, C.G. and Pamer, E.G. 2013. Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13, 790–801.PubMedCentralPubMedCrossRefGoogle Scholar
  6. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  7. Cerf-Bensussan, N. and Gaboriau-Routhiau, V. 2010. The immune system and the gut microbiota: friends or foes? Nat. Rev. Immunol. 10, 735–744.PubMedCrossRefGoogle Scholar
  8. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. 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.PubMedCrossRefGoogle Scholar
  14. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.PubMedCrossRefGoogle Scholar
  22. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  23. Guarner, F. and Malagelada, J.R. 2003. Gut flora in health and disease. Lancet 361, 512–519.PubMedCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. Hooper, L.V., Littman, D.R., and Macpherson, A.J. 2012. Interactions between the microbiota and the immune system. Science 336, 1268–1273.PubMedCrossRefGoogle Scholar
  26. 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
  27. 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.PubMedCrossRefGoogle Scholar
  28. Isolauri, E. 2003. Probiotics for infectious diarrhoea. Gut 52, 436–437.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  31. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  32. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  40. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  41. 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
  42. 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.CrossRefGoogle Scholar
  43. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  45. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  46. Mundy, R., MacDonald, T.T., Dougan, G., Frankel, G., and Wiles, S. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7, 1697–1706.PubMedCrossRefGoogle Scholar
  47. Nava, G.M. and Stappenbeck, T.S. 2011. Diversity of the autochthonous colonic microbiota. Gut Microbes 2, 99–104.PubMedCentralPubMedCrossRefGoogle Scholar
  48. O’Hara, A.M. and Shanahan, F. 2007. Gut microbiota: Mining for therapeutic potential. Clin. Gastroenterol. Hepatol. 5, 274–284.PubMedCrossRefGoogle Scholar
  49. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  50. Philpott, D. and Girardin, S. 2004. The role of toll-like receptors and nod proteins in bacterial infection. Mol. Immunol. 41, 1099–1108.PubMedCrossRefGoogle Scholar
  51. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  52. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  53. 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.PubMedCrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. Shanahan, F. 2002. The host-microbe interface within the gut. Best Pract. Res. Clin. Gastroenterol. 16, 915–931.PubMedCrossRefGoogle Scholar
  56. 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.PubMedCrossRefGoogle Scholar
  57. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. Tanoue, T., Umesaki, Y., and Honda, K. 2010. Immune responses to gut microbiota-commensals and pathogens. Gut Microbes 1, 224–233.PubMedCentralPubMedCrossRefGoogle Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. 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.PubMedCrossRefGoogle Scholar
  63. 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.PubMedCrossRefGoogle Scholar
  64. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  65. 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.PubMedCrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • My Young Yoon
    • 1
    • 3
  • Keehoon Lee
    • 1
    • 2
  • Sang Sun Yoon
    • 1
    • 2
    • 3
    Email author
  1. 1.Department of Microbiology and ImmunologyYonsei University College of MedicineSeoulRepublic of Korea
  2. 2.Brain Korea 21 Project for Medical SciencesYonsei University College of MedicineSeoulRepublic of Korea
  3. 3.Institute for Immunology and Immunological DiseasesYonsei University College of MedicineSeoulRepublic of Korea

Personalised recommendations

Cite article

Buy options