Interactions of the Commensal Flora with the Human Gastrointestinal Tract

James P. Nataro

doi:10.1128/9781555817619.ch13

Chapter 13 : Interactions of the Commensal Flora with the Human Gastrointestinal Tract

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Center for Vaccine Development, Departments of Pediatrics, Medicine, and Microbiology and Immunology, University of Maryland School of Medicine, 685 W. Baltimore St., Baltimore, MD 21201

Content Type: Monograph

Publication Year: 2005

Category: Clinical Microbiology; Bacterial Pathogenesis

Book DOI: 10.1128/9781555817619

Chapter DOI: 10.1128/9781555817619.ch13

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Interactions of the Commensal Flora with the Human Gastrointestinal Tract, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap13-1.gif /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap13-2.gif

Abstract:

This chapter surveys recent information on the roles of the commensal intestinal flora and provides an overview of how the natural symbiosis can be enhanced. The dominant microbial genera of the human gastrointestinal tract include Bacteroides, Bifidobacterium, Eubacterium, Lactobacillus, Clostridium, Fusobacterium, Peptococcus, Peptostreptococcus, Escherichia, and Veillonella. The ability of the commensal flora to persist in the intestinal lumen stands in stark contrast to the abundance and vigor of the intestinal immune system. The intestinal mucosa must maintain a highly selective barrier function, capable of permitting the absorption of highly variable nutrients and the sampling of antigens while excluding pathogenic microorganisms. Just as the presence of the commensal flora is needed to drive the maturation of the immune system, several studies have suggested that the flora is required to establish normal epithelial barrier function. The studies by Gordon and Hooper have illuminated dramatically the contributions of the commensal flora to ontogeny of the intestinal mucosa. The study of health-promoting effects conferred by administration of a live commensal flora, so called probiotic species, has a long but often confusing history. The contribution of the enteric commensal flora to human health is only beginning to be appreciated, and many more studies are required. The availability of molecular approaches will greatly accelerate laboratory investigations, but careful clinical observations are required to ascertain the full scope of these effects.

Citation: Nataro J. 2005. Interactions of the Commensal Flora with the Human Gastrointestinal Tract, p 179-186. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch13

Highlighted Text: Show | Hide

Full text loading...

Figures

Interactions of the Commensal Flora with the Human Gastrointestinal Tract

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817619.chap13-1,webId=/content/author/10.1128/9781555817619.chap13-1,properties={foaf_givenname=James P., foaf_name=James P. Nataro, foaf_surname=Nataro, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817619.chap13-aff1]]}]]

/content/10.1128/9781555817619.chap13.fig13-1

Figure 1

Effects of coculture and preconditioned media on the expression of the global regulator of enteroaggregative E. coli virulence, AggR. Enteroaggregative E. coli strain 042 was cocultivated individually with various enteric bacteria in Luria broth at 37°C to the late log phase. Conditioned media were prepared by cultivating the enteric species, filtering out bacterial growth, and correcting pH and nutrient concentration. The aggR transcript in both experiments was quantitated by real-time reverse transcription-PCR. Values expressed are the number of aggR transcripts in coculture or preconditioned media compared with aggR expression in pure control cultures of 042. aggR expression is enhanced by Enterococcus and Clostridium species and diminished by Lactobacillus and Veillonella species. Reprinted from reference 63 with permission.

10.1128/9781555817619/fig13-1_thmb.gif

10.1128/9781555817619/fig13-1.gif

Figure 1

/content/10.1128/9781555817619.chap13.fig13-2

Figure 2

The commensal enteric flora can confer adverse and/or beneficial effects on human health. These effects are illustrated on a continuum representing the typical abundance of these species. Adapted from reference 15 with permission from the American Society for Nutritional Sciences.

10.1128/9781555817619/fig13-2_thmb.gif

10.1128/9781555817619/fig13-2.gif

Figure 2

References

/content/book/10.1128/9781555817619.chap13

1. Adlerberth, I., 1999. Establishment of a normal intestinal microflora in the newborn infant, p. 63– 78. In L. A. Hanson, and R. H. Yolken (ed.), Probiotics, Other Nutritional Factors, and Intestinal Microflora, vol. 42. Lippincott-Raven Publishers, Philadelphia, Pa.

2. Arvola, T.,, K. Laiho,, S. Torkkeli,, H. Mykkanen,, S. Salminen,, L. Maunula,, and E. Isolauri. 1999. Prophylactic Lactobacillus GG reduces antibiotic-associated diarrhea in children with respiratory infections: a randomized study. Pediatrics 104: e64.

3. Asahara, T.,, K. Shimizu,, K. Nomoto,, T. Hamabata,, A. Ozawa,, and Y. Takeda. 2004. Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157:H7. Infect. Immun. 72: 2240– 2247.

4. Bjorkholm, B. M.,, J. L. Guruge,, J. D. Oh,, A. J. Syder,, N. Salama,, K. Guillemin,, S. Falkow,, C. Nilsson,, P. G. Falk,, L. Engstrand,, and J. I. Gordon. 2002. Colonization of germfree transgenic mice with genotyped Helicobacter pylori strains from a case-control study of gastric cancer reveals a correlation between host responses and HsdS components of type I restriction-modification systems. J. Biol. Chem. 277: 34191– 34197.

5. Borriello, S. P., 2002. The normal flora of the gastrointestinal tract, p. 3– 12. In A. L. Hart,, A. J. Stagg,, H. Graffner,, H. Glise,, P. Falk,, and M. A. Kamm (ed.), Gut Ecology. Martin Dunitz, Ltd., London, United Kingdom.

6. Bourlioux, P.,, B. Koletzko,, F. Guarner,, and V. Braesco. 2003. The intestine and its microflora are partners for the protection of the host: report on the Danone Symposium “The Intelligent Intestine,” held in Paris, June 14, 2002. Am. J. Clin. Nutr. 78: 675– 683.

7. Bry, L.,, P. G. Falk,, T. Midtvedt,, and J. I. Gordon. 1996. A model of host-microbial interactions in an open mammalian ecosystem. Science 273: 1380– 1383.

8. El Asmar, R.,, P. Panigrahi,, P. Bamford,, I. Berti,, T. Not,, G. V. Coppa,, C. Catassi,, and A. Fasano. 2002. Host-dependent zonulin secretion causes the impairment of the small intestine barrier function after bacterial exposure. Gastroenterology 123: 1607– 1615.

9. Freter, R., 1999. Continuous-flow culture models of intestinal microecology, p. 97– 110. In L. Hanson, and R. Yolken (ed.), Probiotics, Other Nutritional Factors, and Intestinal Microflora, vol. 42. Lippincott-Raven, Philadelphia, Pa.

10. Freter, R. 1989. Control mechanisms of the large-intestinal microflora and its influence on the host. Acta Gastroenterol. Latinoam. 19: 197– 217.

11. Freter, R., 1983. Mechanisms that control the microflora in the large intestine, p. 33– 54. In D. J. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, Inc., New York, N.Y.

12. Freter, R.,, H. Brickner,, M. Botney,, D. Cleven,, and A. Aranki. 1983. Mechanisms that control bacterial populations in continuous- flow culture models of mouse large intestinal flora. Infect. Immun. 39: 676– 685.

13. Gibson, G. R. 1999. Dietary modulation of the human gut microflora using the prebiotics oligofructose and inulin. J. Nutr. 129: 1438S– 1441S.

14. Gibson, G. R.,, E. R. Beatty,, X. Wang,, and J. H. Cummings. 1995. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108: 975– 982.

15. Gibson, G. R.,, and M. B. Roberfroid. 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125: 1401– 1412.

16. Gibson, G. R.,, and X. Wang. 1994. Enrichment of bifidobacteria from human gut contents by oligofructose using continuous culture. FEMS Microbiol. Lett. 118: 121– 127.

17. Gionchetti, P.,, F. Rizzello,, A. Venturi,, P. Brigidi,, D. Matteuzzi,, G. Bazzocchi,, G. Poggioli,, M. Miglioli,, and M. Campieri. 2000. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebocontrolled trial. Gastroenterology 119: 305– 309.

18. Gionchetti, P.,, F. Rizzello,, A. Venturi,, and M. Campieri. 2000. Probiotics in infective diarrhoea and inflammatory bowel diseases. J. Gastroenterol. Hepatol. 15: 489– 493.

19. Gordon, J. I.,, L. V. Hooper,, M. S. McNevin,, M. Wong,, and L. Bry. 1997. Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. Am. J. Physiol. Ser. G 273: G565– G570.

20. Helgeland, L.,, J. T. Vaage,, B. Rolstad,, T. Midtvedt,, and P. Brandtzaeg. 1996. Microbial colonization influences composition and T-cell receptor V beta repertoire of intraepithelial lymphocytes in rat intestine. Immunology 89: 494– 501.

21. Hill, M. J. 1991. Bile acids and colorectal cancer: hypothesis. Eur. J. Cancer Prev. 1(Suppl. 2): 69– 74.

22. Hill, M. J. 1997. Intestinal flora and endogenous vitamin synthesis. Eur. J. Cancer Prev. 6( Suppl. 1): S43– S45.

23. Hill, M. J. 1991. The ratio of lithocholic to deoxycholic acid in faeces: a risk factor in colorectal carcinogenesis. Eur. J. Cancer Prev. 1(Suppl. 2): 75– 78.

24. Hooper, L. V.,, L. Bry,, P. G. Falk,, and J. I. Gordon. 1998. Hostmicrobial symbiosis in the mammalian intestine: exploring an internal ecosystem. Bioessays 20: 336– 343.

25. Hooper, L. V.,, P. G. Falk,, and J. I. Gordon. 2000. Analyzing the molecular foundations of commensalism in the mouse intestine. Curr. Opin. Microbiol. 3: 79– 85.

26. Hooper, L. V.,, T. Midtvedt,, and J. I. Gordon. 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22: 283– 307.

27. Hooper, L. V.,, T. S. Stappenbeck,, C. V. Hong,, and J. I. Gordon. 2003. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat. Immunol. 4: 269– 273.

28. Hooper, L. V.,, M. H. Wong,, A. Thelin,, L. Hansson,, P. G. Falk,, and J. I. Gordon. 2001. Molecular analysis of commensal hostmicrobial relationships in the intestine. Science 291: 881– 884.

29. Hooper, L. V.,, J. Xu,, P. G. Falk,, T. Midtvedt,, and J. I. Gordon. 1999. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc. Natl. Acad. Sci. USA 96: 9833– 9838.

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

31. Isolauri, E. 2001. Probiotics in human disease. Am. J. Clin. Nutr. 73: 1142S– 1146S.

32. Isolauri, E. 2000. The use of probiotics in paediatrics. Hosp. Med. 61: 6– 7.

33. Isolauri, E.,, Y. Sutas,, P. Kankaanpaa,, H. Arvilommi,, and S. Salminen. 2001. Probiotics: effects on immunity. Am. J. Clin. Nutr. 73: 444S– 450S.

34. Kalliomaki, M.,, and E. Isolauri. 2003. Role of intestinal flora in the development of allergy. Curr. Opin. Allergy Clin. Immunol. 3: 15– 20.

35. Kalliomaki, M.,, S. Salminen,, H. Arvilommi,, P. Kero,, P. Koskinen,, and E. Isolauri. 2001. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357: 1076– 1079.

36. Kalliomaki, M.,, S. Salminen,, T. Poussa,, H. Arvilommi,, and E. Isolauri. 2003. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 361: 1869– 1871.

37. Kleessen, B.,, B. Sykura,, H. J. Zunft,, and M. Blaut. 1997. Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am. J. Clin. Nutr. 65: 1397– 1402.

38. Kolida, S.,, K. Tuohy,, and G. R. Gibson. 2002. Prebiotic effects of inulin and oligofructose. Br. J. Nutr. 87( Suppl. 2): S193– S197.

39. Krinos, C. M.,, M. J. Coyne,, K. G. Weinacht,, A. O. Tzianabos,, D. L. Kasper,, and L. E. Comstock. 2001. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414: 555– 558.

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

41. MacFarlane, G. T.,, and S. Macfarlane. 1997. Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand. J. Gastroenterol. Suppl. 222: 3– 9.

42. MacFarlane, G. T.,, S. Macfarlane,, and G. R. Gibson. 1998. Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb. Ecol. 35: 180– 187.

43. MacFarlane, G. T.,, and A. J. McBain,. 1999. The human colonic microbiota, p. 1– 25. In G. R. Gibson, and M. Roberfroid (ed.), Colonic Microbiota, Nutrition and Health. Kluwer Academic Publishers, Dortrecht, The Netherlands.

44. MacPherson, A. J.,, and T. Uhr. 2004. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303: 1662– 1665.

45. McBain, A. J.,, and G. T. Macfarlane. 1998. Ecological and physiological studies on large intestinal bacteria in relation to production of hydrolytic and reductive enzymes involved in formation of genotoxic metabolites. J. Med. Microbiol. 47: 407– 416.

46. McBain, A. J.,, and G. T. MacFarlane. 1997. Investigations of bifidobacterial ecology and oligosaccharide metabolism in a three-stage compound continuous culture system. Scand. J. Gastroenterol. Suppl. 222: 32– 40.

47. McBain, A. J.,, and G. T. MacFarlane. 2001. Modulation of genotoxic enzyme activities by non-digestible oligosaccharide metabolism in in-vitro human gut bacterial ecosystems. J. Med. Microbiol. 50: 833– 842.

48. Mehrazar, K.,, A. Gilman-Sachs,, and Y. B. Kim. 1993. Intestinal absorption of immunologically intact macromolecules in germfree colostrum-deprived piglets maintained on total parenteral nutrition. J. Parenter. Enteral Nutr. 17: 8– 15.

49. Mehrazar, K.,, and Y. B. Kim. 1988. Total parenteral nutrition in germfree colostrum-deprived neonatal miniature piglets: a unique model to study the ontogeny of the immune system. J. Parenter. Enteral Nutr. 12: 563– 568.

50. Mills, J. C.,, N. Andersson,, C. V. Hong,, T. S. Stappenbeck,, and J. I. Gordon. 2002. Molecular characterization of mouse gastric epithelial progenitor cells. Proc. Natl. Acad. Sci. USA 99: 14819– 14824.

51. Miranda, R. L.,, T. Conway,, M. P. Leatham,, D. E. Chang,, W. E. Norris,, J. H. Allen,, S. J. Stevenson,, D. C. Laux,, and P. S. Cohen. 2004. Glycolytic and gluconeogenic growth of Escherichia coli O157:H7 (EDL933) and E. coli K-12 (MG1655) in the mouse intestine. Infect. Immun. 72: 1666– 1676.

52. Moore, W. E.,, and L. H. Moore. 1995. Intestinal floras of populations that have a high risk of colon cancer. Appl. Environ. Microbiol. 61: 3202– 3207.

53. Mysorekar, I. U.,, R. G. Lorenz,, and J. I. Gordon. 2002. A gnotobiotic transgenic mouse model for studying interactions between small intestinal enterocytes and intraepithelial lymphocytes. J. Biol. Chem. 277: 37811– 37819.

54. Neish, A. S.,, A. T. Gewirtz,, H. Zeng,, A. N. Young,, M. E. Hobert,, V. Karmali,, A. S. Rao,, and J. L. Madara. 2000. Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 289: 1560– 1563.

55. Pool-Zobel, B. L.,, A. Bub,, U. M. Liegibel,, S. Treptow-van Lishaut,, and G. Rechkemmer. 1998. Mechanisms by which vegetable consumption reduces genetic damage in humans. Cancer Epidemiol. Biomarkers Prev. 7: 891– 899.

56. Rautanen, T.,, E. Isolauri,, E. Salo,, and T. Vesikari. 1998. Management of acute diarrhoea with low osmolarity oral rehydration solutions and Lactobacillus strain GG. Arch. Dis. Child. 79: 157– 160.

57. Rautava, S.,, and E. Isolauri. 2002. The development of gut immune responses and gut microbiota: effects of probiotics in prevention and treatment of allergic disease. Curr. Issues Intest. Microbiol. 3: 15– 22.

58. Rawls, J. F.,, B. S. Samuel,, and J. I. Gordon. 2004. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 101: 4596– 4601.

59. Reid, G.,, M. E. Sanders,, H. R. Gaskins,, G. R. Gibson,, A. Mercenier,, R. Rastall,, M. Roberfroid,, I. Rowland,, C. Cherbut,, and T. R. Klaenhammer. 2003. New scientific paradigms for probiotics and prebiotics. J. Clin. Gastroenterol. 37: 105– 118.

60. Rhee, K. J.,, P. Sethupathi,, A. Driks,, D. K. Lanning,, and K. L. Knight. 2004. Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. J. Immunol. 172: 1118– 1124.

61. Roberfroid, M. B.,, J. A. Van Loo,, and G. R. Gibson. 1998. The bifidogenic nature of chicory inulin and its hydrolysis products. J. Nutr. 128: 11– 19.

62. Roller, M.,, G. Rechkemmer,, and B. Watzl. 2004. Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J. Nutr. 134: 153– 156.

63. Ruiz-Perez, F.,, S. Davis,, and J. Nataro. 2004. Use of a continuous- flow anaerobic culture to characterize enteric virulence gene expression. Infect. Immun. 72: 3793– 3802.

64. Salminen, S.,, C. Bouley,, M. C. Boutron-Ruault,, J. H. Cummings,, A. Franck,, G. R. Gibson,, E. Isolauri,, M. C. Moreau,, M. Roberfroid,, and I. Rowland. 1998. Functional food science and gastrointestinal physiology and function. Br. J. Nutr. 80( Suppl. 1): S147– S171.

65. Sartor, R. B. 2000. Probiotics in chronic pouchitis: restoring luminal microbial balance. Gastroenterology 119: 584– 587.

66. Schaedler, R. W.,, R. Dubos,, and R. Costello. 1965. The development of the bacterial flora in the gastrointestinal tract of mice. J. Exp. Med. 122: 59– 66.

67. Schultz, M.,, and R. B. Sartor. 2000. Probiotics and inflammatory bowel diseases. Am. J. Gastroenterol. 95: S19– S21.

68. Shroff, K. E.,, K. Meslin,, and J. J. Cebra. 1995. Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut. Infect. Immun. 63: 3904– 3913.

69. Sperandio, V.,, J. L. Mellies,, W. Nguyen,, S. Shin,, and J. B. Kaper. 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 96: 15196– 15201.

70. Sperandio, V.,, A. G. Torres,, J. A. Giron,, and J. B. Kaper. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183: 5187– 5197.

71. Srivastava, K. K. 1978. Colonization resistance against potentially pathogenic bacteria in hexaflora-associated gnotobiotic mice. Can. J. Microbiol. 24: 79– 83.

72. Stappenbeck, T. S.,, L. V. Hooper,, J. K. Manchester,, M. H. Wong,, and J. I. Gordon. 2002. Laser capture microdissection of mouse intestine: characterizing mRNA and protein expression, and profiling intermediary metabolism in specified cell populations. Methods Enzymol. 356: 167– 196.

73. Sweeney, N. J.,, P. Klemm,, B. A. McCormick,, E. Moller- Nielsen,, M. Utley,, M. A. Schembri,, D. C. Laux,, and P. S. Cohen. 1996. The Escherichia coli K-12 gntP gene allows E. coli F-18 to occupy a distinct nutritional niche in the streptomycin- treated mouse large intestine. Infect. Immun. 64: 3497– 3503.

74. Umesaki, Y.,, and H. Setoyama. 2000. Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes Infect. 2: 1343– 1351.

75. Van Tassell, R. L.,, D. G. Kingston,, and T. D. Wilkins. 1990. Dietary genotoxins and the human colonic microflora. Prog. Clin. Biol. Res. 340E: 149– 158.

76. Van Tassell, R. L.,, D. G. Kingston,, and T. D. Wilkins. 1990. Metabolism of dietary genotoxins by the human colonic microflora: the fecapentaenes and heterocyclic amines. Mutat. Res. 238: 209– 221.

77. Weisburger, J. H. 2001. Antimutagenesis and anticarcinogenesis, from the past to the future. Mutat. Res. 480- 481: 23– 35.

78. Wong, M. H.,, T. S. Stappenbeck,, and J. I. Gordon. 1999. Living and commuting in intestinal crypts. Gastroenterology 116: 208– 210.

79. Xu, J.,, M. K. Bjursell,, J. Himrod,, S. Deng,, L. K. Carmichael,, H. C. Chiang,, L. V. Hooper,, and J. I. Gordon. 2003. A genomic view of the human- Bacteroides thetaiotaomicron symbiosis. Science 299: 2074– 2076.