Chapter 2 : Role of the Indigenous Microbiota in Health and Disease

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This chapter focuses on the indigenous microbiota of the human large bowel, arguably the best-known ecosystem of the body. The study of microbial communities falls within the domain of microbial ecology—the study of the interrelationships that occur between populations within a community and between the community and the environment in which it is located. Microbial ecology is about how ecosystems work and therefore details the functions of populations, individually and collectively, in nature. The indigenous microbiota is a potent source of opportunistic infections that arise when the mechanisms that normally confine the microbes to a particular site are disrupted. Anaerobic infections following bowel surgery, urinary tract infections, chronic respiratory tract infections, dental/gingival diseases, and annoying skin conditions come into this category. Medical knowledge focuses on the pathogenesis of diseases and the derivation of intervention strategies. To understand health, one must learn about the mechanisms that operate in the healthy body by which stable ecosystems are sustained and maintained. Then, health might be guarded by reason, perhaps by interventions that would produce predictable outcomes on the basis of knowledge of molecular networks. Fortunately, the technological approaches to achieve these goals are at the fingertips of microbiologists: metagenomics to access and assess community genetics, and metabolomics to analyze functional attributes of the indigenous microbiota in concert with that of the host.

Citation: Tannock G. 2008. Role of the Indigenous Microbiota in Health and Disease, p 9-19. In Versalovic J, Wilson M (ed), Therapeutic Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555815462.ch2
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1. Ashelford,, K. E.,, N. A. Chuzhanova,, J. C. Fry,, A. J. Jones, and, A. J. Weightman. 2005. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71: 77247736.
2. Ashelford,, K. E.,, N. A. Chuzhanova,, J. C. Fry,, A. J. Jones, and, A. J. Weightman. 2006. New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl. Environ. Microbiol. 72: 57345741.
3. Backhed,, F.,, H. Ding,, T. Wang,, L. V. Hooper,, G. Y. Koh,, A. Nagy,, C. F. Semenkovich, and, J. I. Gordon. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 101: 1571815723.
4. Bartlett, J. G. 1983. Pseudomembranous colitis, p. 447479. In D. J. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, New York, NY.
5. Bealmear,, P. M.,, M. A. South,, and R. Wilson. 1985. David’s story: the gift of 12 years, 5 months, and 1 day, p. 475–489. In B. S. Wostman and, J. R. Pleasants (ed.), Germfree Research: Microflora Control and Its Application to the Biomedical Sciences. Alan R. Liss, New York, NY.
6. Bibiloni,, R.,, M. Mangold,, K. L. Madsen,, R. N. Fedorak, and, G. W. Tannock. 2006. The bacteriology of biopsies differs between newly diagnosed, untreated, Crohn’s disease and ulcerative colitis patients. J. Med. Microbiol. 55: 11411149.
7. Bik,, E. M.,, P. B. Eckburg,, S. R. Gill,, K. E. Nelson,, E. A. Purdom,, F. Francois,, G. Perez-Perez,, M. J. Blaser, and, D. A. Relman. 2006. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl. Acad. Sci. USA 103: 732737.
8. Cook, G. M., and, J. B. Russell. 1994. Energy spilling reactions of Streptococcus bovis and resistance of its membrane to proton conductance. Appl. Environ. Microbiol. 60: 19421948.
9. Cooperstock, M. S., and, A. J. Zedd. 1983. Intestinal flora of infants, p. 79–99. In D. J. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, New York, NY.
10. Corr,, S. C.,, L. Yin,, C. U. Riedel,, P. W. O’Toole,, C. Hill, and, C. G. M. Gahan. 2007. Bacteriocin production as a mechanism for the anti-infective activity of Lactobacillus salivarius UCC118. Proc. Natl. Acad. Sci. USA 104: 76177621.
11. Cummings, J. H., and, G. T. Macfarlane. 1991. The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 70: 443459.
12. Dubos, R. 1959. Mirage of Health. Utopias, Progress, and Biological Change. Rutgers University Press, New Brunswick, NJ.
13. Dubos, R.,, D. Savage, and, R. Schaedler. 1966. Biological Freudianism: lasting effects of early environmental influences. Pediatrics 38: 789800.
14. Ducluzeau, R., and, P. Raibaud. 1979. Ecologie Microbienne du Tube Digestif. Masson, Paris, France.
15. Eckburg,, P. B.,, E. M. Bik,, C. N. Bernstein,, E. Purdom,, L. Dethlefsen,, M. Sargent,, S. R. Gill,, K. E. Nelson, and, D. A. Relman. 2005. Diversity of the human intestinal microbial flora. Science 308: 16351638.
16. Felske, A.,, H. Rheims,, A. Wolerink,, E. Stackebrandt, and, A. D. L. Akkermans. 1997. Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grassland soils. Microbiology 143: 29832989.
17. Finegold, S. M. 1977. Anaerobic Bacteria in Human Disease. Academic Press, New York, NY.
18. Flint,, H. J.,, S. H. Duncan,, K. P. Scott, and, P. Louis. 2007. Interactions and competition within the microbial community of the human colon: links between diet and health. Environ. Microbiol. 9: 11011111.
19. Freter, R.,, G. D. Abrams, and, A. Aranki. 1973. Patterns of interaction in gnotobiotic mice among bacteria of a synthetic “normal” intestinal flora, p. 429–433. In J. B. Heneghan (ed.), Germfree Research. Academic Press, New York, NY.
20. Fuller, R., and, B. E. Brooker. 1974. Lactobacilli which attach to the crop epithelium of the fowl. Am. J. Clin. Nutr. 27: 13051312.
21. Gill,, S. R.,, M. Pop,, R. T. DeBoy,, P. B. Eckburg,, P. J. Turnbaugh,, B. S. Samuel,, J. I. Gordon,, D. A. Relman,, C. M. Fraser-Liggett, and, K. E. Nelson. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312: 13551359.
22. Gracey, M. 1983. The contaminated small bowel syndrome, p. 495–515. In D. J. Hentges (ed.), Human Intestinal Micro-flora in Health and Disease. Academic Press, New York, NY.
23. Hagen,, K. E.,, L. L. Guan,, G. W. Tannock,, D. R. Korver, and, G. E. Allison. 2005. Detection, characterization, and in vitro and in vivo expression of genes encoding S-proteins in Lactobacillus gallinarum strains isolated from chicken crops. Appl. Environ. Microbiol. 71: 66336643.
24. Handelsman, J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68: 669685.
25. Hardin, G. 1960. The competitive exclusion principle. Science 131: 12921297.
26. Harmsen,, H. J. M.,, A. C. M. Wildeboer,, G. C. Raangs,, A. A. Wagendorp,, N. Klijn,, J. G. Bindels, and, G. W. Welling. 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30: 6167.
27. Hayashi, H.,, R. Takahashi,, T. Nishi,, M. Sakamoto, and, Y. Benno. 2005. Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J. Med. Microbiol. 54: 10931101.
28. Hentges, D. J., and, R. Freter. 1962. In vivo and in vitro antagonism of intestinal bacteria against Shigella flexneri. I. Correlation between various tests. J. Infect. Dis. 110: 3037.
29. Hooper,, L. V.,, M. H. Wong,, A. Thelin,, L. Hansson,, P. G. Falk, and, J. I. Gordon. 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science 291: 881884.
30. 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: 98339838.
31. Hopkin, J. M. 1997. Mechanisms of enhanced prevalence of asthma and atopy in developed countries. Curr. Opin. Immunol. 9: 788792.
32. Hungate, R. E. 1966. The Rumen and Its Microbes. Academic Press, New York, NY.
33. Kell,, D. B.,, M. Brown,, H. M. Davey,, W. B. Dunn,, I. Spasic, and, S. G. Oliver. 2005. Metabolic footprinting and systems biology: the medium is the message. Nat. Rev. 3: 557565.
34. Kimura, K.,, A. L. McCartney,, M. A. McConnell, and, G. W. Tannock. 1997. Analysis of fecal populations of bifidobacteria and lactobacilli and investigation of the immunological responses of their human hosts to the predominant strains. Appl. Environ. Microbiol. 63: 33943398.
35. Konrad, A.,, Y. Cong,, W. Duck,, R. Borlaza, and, C. O. Elson. 2006. Tight mucosal compartmentation of the murine immune response to antigens of the enteric microbiota. Gastroenterology 130: 20502059.
36. Lay,, C.,, L. Rigottier-Gois,, K. Holmstrom,, M. Rajilic,, E. E. Vaughan,, W. M. de Vos,, M. D. Collins,, R. Thiel,, P. Namsolleck,, M. Blaut, and, J. Dore. 2005. Colonic microbiota signatures across five northern European countries. Appl. Environ. Microbiol. 71: 41534155.
37. Lepage,, P.,, P. Seksik,, M. Sutren, M.-F. de la Cochetiere,, R. Jian,, P. Marteau, and, J. Dore. 2005. Biodiversity of the mucosa-associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm. Bowel Dis. 11: 473480.
38. Lodes,, M. J.,, Y. Cong,, C. O. Elson,, R. Mohamath,, C. J. Landers,, S. R. Targan,, M. Fort, and, R. M. Hershberg. 2004. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Investig. 113: 12961306.
39. Macdonald, T. T., and, G. Monteleone. 2005. Immunity, inflammation, and allergy in the gut. Science 307: 19201925.
40. McBee, R. H. 1977. Fermentation in the hindgut, p. 185–222. In R. T. J. Clarke and, T. Bauchop (ed.), Microbial Ecology of the Gut. Academic Press, London, United Kingdom.
41. McCartney, A. L.,, W. Wenzhi, and, G. W. Tannock. 1996. Molecular analysis of the composition of the bifidobacterial and lactobacillus microflora of humans. Appl. Environ. Microbiol. 62: 46084613.
42. Miller, T. L., and, M. J. Wolin. 1983. Stability of Methanobacter smithii populations in the microbial flora excreted from the human large bowel. Appl. Environ. Microbiol. 45: 317318.
43. Moore, W. E. C., and, L. V. Holdeman. 1974. Special problems associated with the isolation and identification of intestinal bacteria in fecal flora studies. Am. J. Clin. Nutr. 27: 14501455.
44. Muyzer, G., and, K. Smalla. 1998. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73: 127141.
45. Nicholson, J. K.,, E. Holmes,, J. C. Lindon, and, I. D. Wilson. 2004. The challenges of modeling mammalian biocomplexity. Nat. Biotechnol. 22: 12681274.
46. Norin,, K. E.,, B. E. Gustafsson,, B. S. Lindblad, and, T. Midtvedt. 1985. The establishment of some microflora associated biochemical characteristics in feces from children during the first years of life. Acta Paediatr. Scand. 74: 207212.
47. Prescott,, S. L.,, C. Macaubus,, B. J. Holt,, T. B. Smallacombe,, R. Loh,, P. D. Sly, and, P. G. Holt. 1998. Transplacental priming of the human immune system to environmental allergens: universal skewing of initial T cell responses toward the Th2 cytokine profile. J. Immunol. 160: 47304737.
48. Prindiville, T.,, M. Cantrell, and, K. H. Wilson. 2004. Ribosomal DNA sequence analysis of mucosa-associated bacteria in Crohn’s disease. Inflamm. Bowel Dis. 10: 824833.
49. Rawls,, J. F.,, M. A. Mahowald,, R. E. Ley, and, J. I. Gordon. 2006. Reciprocal gut microbiota transplants from zebrafish and mice to germfree recipients reveal host habitat selection. Cell 127: 423433.
50. Roberton, A. M., and, A. P. Corfield. 1999. Mucin degradation and its significance in inflammatory conditions of the gastrointestinal tract, p. 222–261. In G. W. Tannock (ed.), Medical Importance of the Normal Microflora. Kluwer Academic Publishers, Dordrecht, The Netherlands.
51. Roediger, W. E. 1980. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21: 793798.
52. Russell, J. B. 2002. Rumen Microbiology and Its Role in Ruminant Nutrition. Cornell University, Ithaca, NY.
53. Russell, J. B., and, G. M. Cook. 1995. Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol. Rev. 59: 4862.
54. Salyers, A. A. 1982. Enzymes involved in degradation of unabsorbed polysaccharides by bacteria of the large bowel, p. 135–138. In G. Wallace and, L. Bell (ed.), Fibre in Human and Animal Nutrition. The Royal Society of New Zealand, Wellington, New Zealand.
55. Sartor,, R. B. 2004. Microbial influences in inflammatory bowel disease: role in pathogenesis and clinical implications, p. 138–162. In R. B. Sartor and, W. J. Sandborn (ed.), Kirstner’s Inflammatory Bowel Diseases. Elsevier Publishers, London, United Kingdom.
56. Schell,, M. A.,, M. Karamirantzou,, B. Snel,, D. Vilanova,, B. Berger,, G. Pessi,, M. C. Zwahlen,, F. Desiere,, P. Bork,, M. Delby, and, R. D. Pridmore. 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. USA 99: 1442214427.
57. Simon,, G. L., and, S. L. Gorbach. 1984. Intestinal flora in health and disease. Gastroenterology 86: 174193.
58. Smith,, K. D.,, E. Andersen-Nissen,, F. Hayashi,, K. Strobe,, M. A. Bergman,, S. L. Rassoulian Barrett,, B. T. Cookson, and, A. Aderem. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4: 12471253.
59. Snart,, J.,, R. Bibiloni,, T. Grayson,, C. Lay,, H. Zhang,, G. E. Allison,, J. K. Laverdiere,, F. Temelli,, T. Vasanthan,, R. Bell, and, G. W. Tannock. 2006. Supplementation of the diet with high-viscosity beta-glucan results in enrichment for lactobacilli in the rat cecum. Appl. Environ. Microbiol. 72: 19251931.
60. Stappenbeck,, T. S.,, L. V. Hooper, and, J. I. Gordon. 2002. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 99: 1545115455.
61. Suau,, A.,, R. Bonnet,, M. Sutren,, J.-J. Godon,, G. R. Gibson,, M. D. Collins, and, J. Dore. 1999. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65: 47994807.
62. Swidsinski,, A.,, A. Ladhoff,, A. Pernthaler,, S. Swidsinski,, V. Loening-Baucke,, M. Ortner,, J. Weber,, U. Hoffman,, S. Schreiber,, M. Dietel, and, H. Lochs. 2002. Mucosal flora in inflammatory bowel disease. Gastroenterology 122: 4454.
63. Tannock,, G. W. 1984. Control of gastrointestinal pathogens by normal flora, p. 374–382. In M. J. Klug and, C. A. Reddy (ed.), Perspectives in Microbial Ecology. American Society for Microbiology, Washington, DC.
64. Tannock,, G. W. 1992. The lactic microflora of pigs, mice and rats, p. 21–48. In J. B. Wood (ed.), The Lactic Acid Bacteria, vol. 1. The Lactic Acid Bacteria in Health and Disease. Elsevier Applied Science, London, United Kingdom.
65. Tannock,, G. W. 1995. Normal Microflora. An Introduction to Microbes Inhabiting the Human Body. Chapman and Hall, London, United Kingdom.
66. Tannock,, G. W. 1997. Influences of the normal microbiota on the animal host, p. 466–497. In R. I. Mackie,, B. A. White, and, R. E. Isaacson (ed.), Gastrointestinal Microbiology, vol. 2. Gastrointestinal Microbes and Host Interactions. Chapman and Hall, New York, NY.
67. Tannock,, G. W. 2003. The intestinal microflora, p. 1–23. In R. Fuller and, G. Perdigon (ed.), Gut Flora. Nutrition, Immunity and Health. Blackwell Press, Oxford, United Kingdom.
68. Tannock,, G. W. 2004. A special fondness for lactobacilli. Appl. Environ. Microbiol. 70: 31893194.
69. Tannock,, G. W. 2005. Microbiota of mucosal surfaces in the gut of monogastric animals, p. 163–178. In J. P. Nataro,, P. S. Cohen,, H. L., T. Mobley, and, J. N. Weiser (ed.), Colonization of Mucosal Surfaces. ASM Press, Washington, DC.
70. Tannock,, G. W.,, S. Ghazally,, J. Walter,, D. Loach,, H. Brooks,, G. Cook,, M. Surette,, C. Simmers,, P. Bremer,, F. Dal Bello, and, C. Hertel. 2005. Ecological behavior of Lactobacillus reuteri 100–23 is affected by mutation of the luxS gene. Appl. Environ. Microbiol. 71: 84198425.
71. Tannock,, G. W.,, K. Munro,, R. Bibiloni,, M. A. Simon,, P. Hargreaves,, P. Gopal,, H. Harmsen, and, G. Welling. 2004. Impact of consumption of oligosaccharide-containing biscuits on the fecal microbiota of humans. Appl. Environ. Microbiol. 70: 21292136.
72. Tannock,, G. W.,, K. Munro,, H. J., M. Harmsen,, G. W. Welling,, J. Smart, and, P. K. Gopal. 2000. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl. Environ. Microbiol. 66: 25782588.
73. Targan,, S. R.,, C. J. Landers,, H. Yang,, M. J. Lodes,, Y. Cong,, K. A. Papadakis,, E. Vasiliauskas,, C. O. Elson, and, R. M. Hershberg. 2005. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn’s disease. Gastroenterology 128: 20202028.
74. Van der Waaij, D.,, J. M. Berghuis de Vries, and, J. E. C. Lekkerkerk. 1971. Colonisation resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. 69: 405411.
75. Van der Waaij,, L.,, H. J. M. Harmsen,, M. Madjipour,, F. G., M. Kroese,, M. Zwiers,, H. M. van Dullemen,, N. K. de Boer,, G. W. Welling, and, P. L. M. Jansen. 2005. Bacterial population analysis of human colon and terminal ileum biopsies with 16S rRNA-based fluorescent probes: commensal bacteria live in suspension and have no direct contact with epithelial cells. Inflamm. Bowel Dis. 11: 865871.
76. Van der Werf,, M. J.,, R. H. Jellema, and, T. Hankemeier. 2005. Microbial metabolomics: replacing trial-and-error by the unbiased selection and ranking of targets. J. Ind. Microbiol. Biotechnol. 32: 234252.
77. Walter,, J.,, P. Chagnaud,, G. W. Tannock,, D. M. Loach,, F. Dal Bello,, H. F. Jenkinson,, W. P. Hammes, and, C. Hertel. 2005. A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl. Environ. Microbiol. 71: 979986.
78. Walter,, J.,, N. C. K. Heng,, W. P. Hammes,, D. M. Loach,, G. W. Tannock, and, C. Hertel. 2003. Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl. Environ. Microbiol. 69: 20442051.
79. Walter,, J.,, D. M. Loach,, M. Alqumber,, C. Rockel,, C. Hermann,, M. Pfitzenmaier, and, G. W. Tannock. 2007. D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100–23 results in impaired colonization of the mouse gastrointestinal tract. Environ. Microbiol. 9: 17501760.
80. Wang, M.,, S. Ahrne,, B. Jeppsson, and, G. Molin. 2005. Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol. Ecol. 54: 219231.
81. Wilson, M. 2005. Microbial Inhabitants of Humans: Their Ecology and Role in Health and Disease. Cambridge University Press, New York, NY.
82. 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: 20742076.
83. Yabuhara,, A.,, C. Macaubas,, S. L. Prescott,, T. J. Venaille,, B. J. Holt,, W. Habre,, P. D. Sly, and, P. G. Holt. 1997. Th2-polarized immunological memory to inhalant allergens in atopics is established during infancy and early childhood. Clin. Exp. Allergy 27: 12371239.
84. Yuki,, N.,, T. Shimazaki,, A. Kushiro,, K. Watanabe,, K. Uchida,, T. Yuyama, and, M. Morotomi. 2000. Colonization of the stratified squamous epithelium of the nonsecreting area of horse stomach by lactobacilli. Appl. Environ. Microbiol. 66: 50305034.
85. Zoetendal,, E. G.,, A. D. Akkermans, and, W. M. de Vos. 1998. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host specific communities of active bacteria. Appl. Environ. Microbiol. 64: 38543859.
86. Zoetendal,, E. G.,, A. von Wright,, T. Vilpponen-Samela,, K. Ben-Amor,, A. D. Akkermans, and, W. M. De Vos. 2002. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl. Environ. Microbiol. 68: 34013407.

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