Skip to main content Accessibility help
×
Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T00:03:57.712Z Has data issue: false hasContentIssue false

12 - Bacterial Growth on Mucosal Surfaces and Biofilms in the Large Bowel

Published online by Cambridge University Press:  23 November 2009

S. Macfarlane
Affiliation:
MRC Microbiology and Gut Biology Group, University of Dundee, Ninewells Hospital Medical School, Dundee, UK
G. T. Macfarlane
Affiliation:
MRC Microbiology and Gut Biology Group, University of Dundee, Ninewells Hospital Medical School, Dundee, UK
Michael Wilson
Affiliation:
University College London
Deirdre Devine
Affiliation:
Leeds Dental Institute, University of Leeds
Get access

Summary

THE LARGE INTESTINAL MICROBIOTA

It has been estimated that of the 1014 cells associated with the human body, approximately 90 per cent are microorganisms, and the vast majority of these organisms are bacteria growing in the large intestine (Savage, 1977). The large bowel is the main area of permanent microbial colonisation of the human gastrointestinal tract; gastric acid kills most oral and environmental microorganisms in the stomach, whereas the rapid passage of digestive materials through the upper gut does not allow time for significant bacterial growth to occur (Macfarlane and Cummings, 1991). However, the rate of movement of intestinal contents slows markedly in the large gut, which facilitates development of rich and diverse bacterial communities (Cummings, 1978; Cummings et al., 1993). The growth and metabolic activities of these microbial populations are influenced to a considerable degree by diet, as well as by the structure and physiology of the colon (Macfarlane et al., 1995).

The large intestine is an open system in the sense that food residues from the small intestine enter at one end and, together with bacterial cell mass, are excreted at the other end. Because of this, the colon is often viewed as being a continuous culture system, although only the caecum and ascending colon really exhibit characteristics of a continuous culture (Cummings et al., 1987; Macfarlane, Macfarlane, and Gibson, 1998).

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2003

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adlerberth, I., Ahrne, S., Johansson, M.-L., Molin, G., Hanson, L. A. and Wold, A. E. (1996). A mannose-specific adherence mechanism in Lactobacillus plantarum conferring binding to the human colonic cell line HT-29. Applied and Environmental Microbiology, 62, 2244–2251Google ScholarPubMed
Anwar, H., Dasgupta, M. K. and Costerton, J. W. (1990). Testing the susceptibility of bacteria in biofilms to antibacterial agents. Antimicrobial Agents and Chemotherapy, 34, 2043–2046CrossRefGoogle ScholarPubMed
Beech, I. B., Paiva, M., Caus, M. and Coutinho, C. M. L. (2001). Enzymatic activity within biofilms of sulphate-reducing bacteria. In Biofilm Community Interactions: Chance or Necessity? eds. P. Gilbert, D. Allison, M. Brading, J. Verran and J. Walker, pp. 231–239. Cardiff: Bioline
Bernet, M.-F., Brassart, D., Neeser, J.-R. and Servin, A. L. (1993). Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Applied and Environmental Microbiology, 59, 4121–4128Google ScholarPubMed
Bernet, M.-F., Brassart, D., Neeser, J.-R. and Servin, A. L. (1994). Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut, 35, 483–489CrossRefGoogle ScholarPubMed
Bradley, H. K., Wyatt, G. M. and Bayliss, C. E. (1987). Instability in the faecal flora of a patient suffering from food-related irritable bowel syndrome. Medical Microbiology, 23, 29–32CrossRefGoogle ScholarPubMed
Breznak, J. A. and Pankratz, H. S. (1977). In situ morphology of the gut microbiota of wood eating termites [Reticulitennes flaviceps Kollar and Coptotermes formosanus Shiraki]. Applied and Environmental Microbiology, 33, 406–426Google Scholar
Chadwick, V. S., (1991). Etiology of chronic ulcerative colitis and Crohn's disease. In The Large Intestine: physiology, Pathophysiology and Disease, eds. S. F. phillips, J. H. Pemberton and R. G. Shorter, pp. 445–463. New York: Raven Press
Cohen, M. B. and Giannella, R. A. (1991). Bacterial infections: pathophysiology, clinical features and treatment. In The Large Intestine: physiology, Pathophysiology and Disease, eds. S. F. phillips, J. H. Pemberton and R. G. Shorter, pp. 395–428. New York: Raven Press
Conrad, R., phelps, T. J. and Zeikus, J. G. (1985). Gas metabolism evidence in support of the juxtaposition of hydrogen-producing and methanogenic bacteria in sewage sludge and lake sediments. Applied and Environmental Microbiology, 50, 595–601Google ScholarPubMed
Crociani, J., Grill, J.-P., Huppert, M. and Ballongue, J. (1995). Adhesion of different bifidobacteria strains to human enterocyte-like Caco-2 cells and comparison with in vivo study. Letters in Applied Microbiology, 21, 146–148CrossRefGoogle ScholarPubMed
Croucher, S. C., Houston, A. P., Bayliss, C. E. and Turner, R. J. (1983). Bacterial populations associated with different regions of the human colon wall. Applied and Environmental Microbiology, 45, 1025–1033Google ScholarPubMed
Cummings, J. H. (1978). Diet and transit through the gut. Journal of Plant Foods, 3, 83–95CrossRefGoogle Scholar
Cummings, J. H., Bingham, S. A., Heaton, K. W. and Eastwood, M. A. (1993). Fecal weight, colon cancer risk and dietary intake of non-starch polysaccharides (dietary fiber). Gastroenterology, 103, 1783–1789CrossRefGoogle Scholar
Cummings, J. H. and Macfarlane, G. T. (2001). Is there a role for microorganisms? In Questions and Uncertainties in Inflammatory Bowel Disease, eds. D. P. Jewell, N. Mortensen and B. F. Warren, pp. 42–51. Oxford: Blackwell Science
Cummings, J. H., Pomare, E. W., Branch, W. J., Naylor, C. P. E. and Macfarlane, G. T. (1987). Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut, 28, 1221–1227CrossRefGoogle ScholarPubMed
Dehio, M., Gomez-Duarte, O. G., Dehio, C. and Meyer, T. F. (1998). Vitronectin-dependent invasion of epithelial cells by Neisseria gonorrhoea involves alpha(ⅴ) integrin receptors. FEBS Letters, 424, 84–88CrossRefGoogle Scholar
Simone, C., Ciardi, A., Grassi, A., Gardini, Lambert S., Tzantzoglou, S., Trinchieri, V., Moretti, S. and Jirillo, E. (1992). Effect of Bifidobacterium bifidum and Lactobacillus acidophilus on gut mucosa and peripheral blood B lymphocytes. Immunopharmacology and Immunotoxicology, 14, 331–340CrossRefGoogle ScholarPubMed
De Vuyst, L. and Vandamme, E. J. (1994). Antimicrobial potential of lactic acid bacteria. In Bacteriocins of Lactic Acid Bacteria, eds. L. De Vuyst and E. J. Vandamme, pp. 91–142. Glasgow: Blackie Academic and ProfessionalCrossRef
Dodd, H. M. and Gasson, M. J. (1994). Bacteriocins of lactic acid bacteria. In Genetics and Biotechnology of Lactic Acid Bacteria, eds. M. J. Gasson and W. M. de Vos, pp. 211–251. Glasgow: Blackie Academic and ProfessionalCrossRef
Duensing, T. D., Wing, J. S. and Putten, J. P. M. (1999). Sulfated polysaccharide-directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenisis. Infection and Immunity, 67, 4463–4468Google Scholar
Edmiston, C. E. Jr., Avant, G. R. and Wilson, F. A. (1982). Anaerobic bacterial populations on normal and diseased human biopsy tissue obtained at colonoscopy. Applied Environmental Microbiology, 43, 1173–1181Google ScholarPubMed
Finegold, S. M., Flora, D. J., Attlebury, H. R. and Sutter, L. V. (1975). Fecal bacteriology of colonic polyp patients and control patients. Cancer Research, 35, 3407–3417Google ScholarPubMed
Finegold, S. M., Sutter, V. L. and Mathisen, G. E. (1983). Normal indigenous intestinal flora. In Human Intestinal Microflora in Health and Disease, ed. D. J. Hentges, pp. 3–31. London: Academic PressCrossRef
Gibson, G. R. (1990). physiology and ecology of the sulphate-reducing bacteria. Journal of Applied Bacteriology, 69, 769–797CrossRefGoogle ScholarPubMed
Gibson, G. R., Cummings, J. H. and Macfarlane, G. T. (1988). Competition for hydrogen between sulphate-reducing bacteria and methanogenic bacteria from the human large intestine. Journal of Applied Bacteriology, 65, 241–247CrossRefGoogle ScholarPubMed
Gibson, G. R., Cummings, J. H. and Macfarlane, G. T. (1991). Growth and activities of sulphate-reducing bacteria in gut contents from healthy subjects and patients with ulcerative colitis. FEMS Microbiology Ecology, 86, 103–112CrossRefGoogle Scholar
Gibson, G. R. and Wang, X. (1994). Regulatory effects of bifidobacteria on the growth of other colonic bacteria. Journal of Applied Bacteriology, 77, 412–420CrossRefGoogle ScholarPubMed
Gibson, S. A. W., McFarlan, C., Hay, S. and Macfarlane, G. T. (1989). Significance of the microflora in proteolysis in the colon. Applied and Environmental Microbiology, 55, 679–683Google ScholarPubMed
Hill, M. J. (1986). The possible role of bacteria in inflammatory bowel disease. Current Concepts in Gastroenterology, 3, 10–14Google Scholar
Hopkins, M. J., Sharp, R. and Macfarlane, G. T. (2001). Age and disease-related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance and community cellular fatty acid profiles. Gut, 48, 198–205CrossRefGoogle ScholarPubMed
Johansson, M.-L., Molin, G., Jeppsson, B., Nobaek, B., Ahrne, S. and Bengmark, S. (1993). Administration of different Lactobacillus strains in fermented oatmeal soup: in vivo colonization of human intestinal mucosa and effect on the indigenous flora. Applied and Environmental Microbiology, 59, 15–20Google ScholarPubMed
Kolenbrander, P. E. (1989). Surface recognition among oral bacteria: multigeneric coaggregations and their mediators. Critical Reviews in Microbiology, 17, 137–159CrossRefGoogle ScholarPubMed
Laukova, A. and Czikkova, S. (1998). Inhibition effect of enterocin CCM 4231 in the rumen fluid environment. Letters in Applied Microbiology, 26, 215–218CrossRefGoogle ScholarPubMed
Lee, A. (1980). Normal flora of animal intestinal surfaces. In Adsorption of Microorganisms to Surfaces, eds. G. Bitton and K. C. Marshall, pp. 145–174. New York: John Wiley & Sons
Lee, F. D., Kraszewski, A., Gordon, J., Howie, J. G. R., McSeveney, D. and Harland, W. A. (1971). Intestinal spirochaetosis. Gut, 12, 126–133CrossRefGoogle ScholarPubMed
Lejeune, R., Callewaert, R., Crabbe, K. and Vuyst, L. (1998). Modelling the growth and bacteriocin production by Lactobacillus amylovorus DCE 471 in batch cultivation. Journal of Applied Microbiology, 84, 159–168CrossRefGoogle Scholar
Macfarlane, G. T. (1991). Fermentation reactions in the large intestine. In Short-Chain Fatty Acids: Metabolism and Clinical Importance, eds. J. H. Cummings, J. L. Rombeau and T. Sakata, pp. 5–10. Columbus: Ross Laboratories Press
Macfarlane, G. T. and Cummings, J. H. (1991). The colonic flora, fermentation and large bowel digestive function. In The Large Intestine: physiology, Pathophysiology and Disease, eds. S. F. phillips, J. H. Pemberton and R. G. Shorter, pp. 51–92. New York: Raven Press
Macfarlane, G. T. and Cummings, J. H. (2002). Diet and the metabolism of intestinal bacteria. In Food Allergy and Intolerance, 2nd ed. (eds. Brostoff, J., Challacombe, S. J., Kniker, W. T.). W.B. Saunders Company Ltd., London, pp. 321–343
Macfarlane, G. T., Cummings, J. H. and Allison, C. (1986). Protein degradation by human intestinal bacteria. Journal of General Microbiology, 132, 1647–1656Google ScholarPubMed
Macfarlane, G. T. and Gibson, G. R. (1991). Formation of glycoprotein degrading enzymes by Bacteroides fragilis. FEMS Microbiology Letters, 77, 289–294CrossRefGoogle Scholar
Macfarlane, G. T. and Gibson, G. R. (1994). Metabolic activities of the normal colonic flora. In Human Health: The Contribution of Microorganisms, ed. S. A. W. Gibson, pp. 17–52. London: Springer-VerlagCrossRef
Macfarlane, G. T. and Gibson, G. R. (1995). Bacterial infections and diarrhea. In Human Colonic Bacteria: Role in Nutrition, physiology and Pathology, eds. G. R. Gibson and G. T. Macfarlane, pp. 201–226. Boca Raton: CRC Press
Macfarlane, G. T. and Gibson, G. R. (1996). Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In Ecology and physiology of Gastrointestinal Microbes Vol. 1: Gastrointestinal Fermentations and Ecosystems, eds. R. I. Mackie and B. A. White, pp. 269–318. New York: Chapman & Hall
Macfarlane, G. T., Gibson, G. R. and Cummings, J. H. (1992). Comparison of fermentation reactions in different regions of the human colon. Journal of Applied Bacteriology, 72, 57–64CrossRefGoogle ScholarPubMed
Macfarlane, G. T., Gibson, G. R., Drasar, B. S. and Cummings, J. H. (1995). Metabolic significance of the colonic microflora. In Gastrointestinal and Oesophageal physiology, ed. R. Whitehead, pp. 249–274. Edinburgh: Churchill Livingstone
Macfarlane, G. T. and Macfarlane, S. (1995). Human intestinal biofilm communities. In The Life and Death of Biofilm, eds. J. Wimpenny, P. Handley, P. Gilbert and H. Lappin-Scott, pp. 83–89. Cardiff: Bioline
Macfarlane, G. T., Macfarlane, S. and Gibson, G. R. (1998). Use of a three-stage compound continuous culture system to investigate bacterial growth and metabolism in the human colonic microbiota. Microbial Ecology, 35, 180–187CrossRefGoogle Scholar
Macfarlane, S., Cummings, J. H. and Macfarlane, G. T. (1999). Bacterial colonisation of surfaces in the large intestine. In Colonic Microflora, Nutrition and Health, eds. G. R. Gibson and M. Roberfroid, pp. 71–87. London: Chapman & HallCrossRef
Macfarlane, S. and Macfarlane, G. T. (2001). Community structure and interactions in the large intestine. In Biofilm Community Interactions: Chance or Necessity? eds. P. Gilbert, D. Allison, M. Brading, J. Verran and J. Walker, pp. 83–96. Cardiff: Bioline
Macfarlane, S., McBain, A. J. and Macfarlane, G. T. (1997). Consequences of biofilm and sessile growth in the large intestine. Advances in Dental Research, 11, 59–68CrossRefGoogle ScholarPubMed
McCabe, K., Mann, M. D. and Bowie, M. D. (1998). D-Lactate production and [14C] succinic acid uptake by adherent and nonadherent Escherichia coli. Infection and Immunity, 66, 907–911Google ScholarPubMed
Meghrous, J., Euloge, P., Junelles, A. M., Ballongue, J. and Petitdemange, H. (1990). Screening of Bifidobacterium strains for bacteriocin production. Biotechnology Letters, 12, 575–580CrossRefGoogle Scholar
Moore, W. E. C. and Holdeman, L. V. (1974). Human fecal flora. The normal flora of 20 Japanese-Hawaiians. Applied Environmental Microbiology, 27, 961–979Google ScholarPubMed
Monteiro, E., Fossey, J., Shiner, M., Drasar, B. S. and Allison, A. C. (1971). Antibacterial antibodies in rectal and colonic mucosa in ulcerative colitis. Lancet, 6(1), 249–251CrossRefGoogle Scholar
Mozes, N. and Rouxhet, P. G. (1992). Influence of surfaces on microbial activity. In Biofilms-Science and Technology, eds. L. F. Melo, T. R. Bott and B. Capdeville, pp. 125–136. Dordrecht: Kluwer Academic PublishersCrossRef
Namavar, F., Theunissen, E. B., Vught, Verweij-Van A. M., Peerbooms, P. G., Bal, M., Hoitsma, H. F. and Maclaren, D. M. (1989). Epidemiology of the Bacteroides fragilis group in the colonic flora in 10 patients with colonic cancer. Journal of Medical Microbiology, 29, 171–176CrossRefGoogle ScholarPubMed
Nelson, D. P. and Mata, L. J. (1970). Bacterial flora associated with the human gastrointestinal mucosa. Gastroenterology, 58, 56–61Google ScholarPubMed
Newton, D. F., Cummings, J. H., Macfarlane, S. and Macfarlane, G. T. (1998). Growth of a human intestinal Desulfovibrio desulfuricans in continuous cultures containing defined populations of saccharolytic and amino acid fermenting bacteria. Journal of Applied Microbiology, 85, 372–380CrossRefGoogle ScholarPubMed
Onderdonk, A. B. (1983). Role of the intestinal microflora in ulcerative colitis. In Human Intestinal Microflora in Health and Disease, ed. D. J. Hentges, pp. 481–493. London: Academic PressCrossRef
Onderdonk, A. B. and Bartlett, M. D. (1979). Bacteriological studies of experimental ulcerative colitis. American Journal of Clinical Nutrition, 32, 258–265CrossRefGoogle ScholarPubMed
O'Riordan, K. C., Condon, S. and Fitzgerald, G. F. (1995). Bacterial interference by Bifidobacterium species and a comparative analysis of genomic profiles from strains of this genus. Proceedings of the Lactic Acid Bacteria Conference, Cork, Ireland, p. 207
Patti, J. M., Allen, B. L., McGavin, M. J. and Hook, M. (1994). MSCRAMM-mediated adherence of microorganisms to host tissues. Annual Review in Microbiology, 48, 585–617CrossRefGoogle ScholarPubMed
Perdigon, G., Medici, M., Jorrat, Bibas Bonet M. E., Budeguer, M. V. and Ruiz Holgado, Pesce A. (1993). Immunomodulating effects of lactic acid bacteria on mucosal and tumoral immunity. International Journal of Immunotherapy, IX, 29–52Google Scholar
Poxton, I. R., Brown, R., Sawyerr, A. and Ferguson, A. (1997). Mucosa-associated bacterial flora of the human colon. Journal of Medical Microbiology, 46, 85–91CrossRefGoogle ScholarPubMed
Pullan, R. D., Thomas, G. A. O., Rhodes, M., Newcombe, R. G., Williams, G. T., Allen, A. and Rhodes, J. (1994). Thickness of adherent mucus gel on colonic mucosa in humans and its relevance to colitis. Gut, 35, 353–359CrossRefGoogle ScholarPubMed
Rembacken, B. J., Snelling, A. M., Hawkey, P. M., Chalmers, D. M. and Axon, A. T. R. (1999). Non-pathogenic Escherichia coli versus mesalzine for the treatment of ulcerative colitis: a randomised trial. Lancet, 354, 635–639CrossRefGoogle Scholar
Roediger, W. E. W. (1980). Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa of man. Gut, 21, 793–798CrossRefGoogle Scholar
Salmond, G. P. C., Bycroft, B. W., Stewart, G. S. A. B. and Williams, P. (1995). The bacterial ‘enigma’: cracking the code of cell–cell communication. Molecular Microbiology, 16, 615–624CrossRefGoogle ScholarPubMed
Sato, J., Mochizuki, K. and Homma, N. (1982). Affinity of the Bifidobacterium to intestinal mucosal epithelial cells. Bifidobacteria Microflora, 1, 51–54Google Scholar
Savage, D. C. (1977). Microbial ecology of the gastrointestinal tract. Annual Review in Microbiology, 31, 107–133CrossRefGoogle ScholarPubMed
Savage, D. C. (1978). Factors involved in colonization of the gut epithelial surface. American Journal of Clinical Nutrition, 31, S131–S135CrossRefGoogle ScholarPubMed
Schiffrin, E. J., Brassart, D., Servin, A. L., Rochat, F. and Donnet-Hughes, A. (1997). Immune modulation of blood leukocytes in humans by lactic acid bacteria: criteria for strain selection. American Journal of Clinical Nutrition, 66, 15S–20SCrossRefGoogle ScholarPubMed
Sharp, R. and Ziemer, C. J. (1999). Application of taxonomy and systematics to molecular techniques in intestinal microbiology. In Colonic Microflora, Nutrition and Health, eds. G. R. Gibson and M. Roberfroid, pp. 167–190. London: Chapman & HallCrossRef
Standiford, T. K., Arenberg, D. A. and Danforth, J. M. (1994). Lipoteichoic acid induces secretion of interleukin-8 from human blood monocytes: a cellular and molecular analysis. Infection and Immunity, 62, 119–25Google ScholarPubMed
Takeuchi, A., Jervis, H. R., Nakagawa, H. and Robinson, D. M. (1974). Spiral-shaped organisms on the surface colonic epithelium of the monkey and man. American Journal of Clinical Nutrition, 27, 1287–1296CrossRefGoogle ScholarPubMed
Loosdrecht, M. C. M., Lyklema, J., Norde, W. and Zehnder, A. J. B. (1990). Influence of interfaces on microbial activity. Microbiological Reviews, 54, 75–87Google ScholarPubMed
Wallace, R. J., Cheng, K.-J., Dinsdale, D. and Orskov, E. R. (1979). An independent microbial flora of the epithelium and its role in the microbiology of the rumen. Nature, 279, 424–426CrossRefGoogle Scholar
Wilkins, T. D. (1981). Microbiological considerations in interpretation of data obtained from experimental animals. Banbury Report, 7, 3–9Google Scholar
Young, G. P., (1991). Butyrate and the molecular biology of the large bowel. In Short Chain Fatty Acids: Metabolism and Clinical Importance, eds. J. H. Cummings, J. L. Rombeau and T. Sakata, pp. 39–44. Columbus: Ross Laboratories Press

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×