Skip to main content Accessibility help
×
Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-22T02:26:24.496Z Has data issue: false hasContentIssue false

18 - Sulphate-reducing bacteria and the human large intestine

Published online by Cambridge University Press:  22 August 2009

Larry L. Barton
Affiliation:
University of New Mexico
W. Allan Hamilton
Affiliation:
University of Aberdeen
Get access

Summary

THE HUMAN LARGE INTESTINAL ECOSYSTEM

The adult human colon typically contains over 200 g of digestive material (Banwell et al., 1981; Cummings et al., 1990; 1992), with the average daily output of faeces in Western countries being approximately 120 g (Cummings et al., 1992). A large proportion of this is microbial cell mass with bacteria comprising approximately 55% of faecal solids in persons living on Western-style diets (Stephen and Cummings, 1980). 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 proximal bowel really exhibits characteristics of a continuous culture.

The large intestine is a complex microbial ecosystem in which bacteria exist in a multiplicity of microhabitats and metabolic niches. The microbiota comprises several hundred bacterial species, subspecies and biotypes. Microbial cell counts are generally in the region of 1011–1012 per gram of gut contents. Some organisms occur in higher numbers than others, but about 40 species make up approximately 99% of all readily culturable isolates (Finegold et al., 1983). Viable counting indicates that bacteria belonging to the genera Bacteroides, Bifidobacterium and Eubacterium, together with a variety of anaerobic Gram-positive rods and cocci predominate in the gut (Finegold et al., 1983), however, molecular methods of analysis indicate that other groups are also numerically important, including atopobium, faecalibacterium and clostridia belonging to the C. coccoides group (Harmsen et al., 2002).

Type
Chapter
Information
Sulphate-Reducing Bacteria
Environmental and Engineered Systems
, pp. 503 - 522
Publisher: Cambridge University Press
Print publication year: 2007

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

Babidge, W., Millard, S. and Roediger, W. E. W. (1998). Sulfides impair short chain fatty acid beta-oxidation at acyl-CoA dehydrogenase level in colonocytes: implications for ulcerative colitis. Mol. Cell. Biochem., 18, 117–24CrossRefGoogle Scholar
Banwell, J. G., Branch, W. J. and Cummings, J. H. (1981). The microbial mass in the human large intestine. Gastroenterology, 80, 1104.Google Scholar
Beerens, H. and Romond, C. (1977). Sulphate-reducing anaerobic bacteria in human feces. Am. J. Clin. Nutr., 30, 1770–6CrossRefGoogle Scholar
Boopathy, R., Robichaux, M., LaFont, D. and Howell, M. (2002). Activity of sulphate-reducing bacteria in human periodontal pocket. Can. J. Microbiol., 48, 1099–103CrossRefGoogle Scholar
Christl, S., Eisner, H. D., Kasper, H. and Scheppach, W. (1996). Antagonistic effects of sulfide and butyrate on proliferation of colonic mucosa: a potential role for these agents in the pathogenesis of ulcerative colitis. Dig. Dis. Sci. 41, 2477–81CrossRefGoogle ScholarPubMed
Christl, S. U., Murgatroyd, P. R., Gibson, G. R. and Cummings, J. H. (1992). Production, metabolism and excretion of hydrogen in the large intestine. Gastroenterology, 102, 1269–77CrossRefGoogle ScholarPubMed
Cummings, J. H., Banwell, J. G., Englyst, H. N., Coleman, N., Segal, I. and Bersohn, D. (1990). The amount and composition of large bowel contents. Gastroenterology, 98, A408.Google Scholar
Cummings, J. H., Bingham, S. A., Heaton, K. W. and Eastwood, M. A. (1992). Fecal weight, colon cancer risk, and dietary intake of nonstarch polysaccharides (dietary fiber). Gastroenterology, 103, 1783–9CrossRefGoogle Scholar
Cummings, J. H. and Macfarlane, G. T. (1991). The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol., 70, 443–59CrossRefGoogle ScholarPubMed
Deplancke, B., Finster, K., Graham, W. V.et al. (2003). Gastrointestinal and microbial responses to sulphate-supplemented drinking water in mice. Exp. Biol. Med., 228, 424–33CrossRefGoogle Scholar
Dzierzewicz, Z., Cwalina, B., Weglarz, L., Wisniowska, B. and Szczerba, J. (2004). Med. Sci. Mon., 10, 185–90
Etterlin, C., McKeowen, A., Bingham, S. A.et al. (1992). D-lactate and acetate as markers of fermentation in man. Gastroenterology, 102, A551.Google Scholar
Finegold, S. M., Sutter, V. L. and Mathisen, G. E. (1983). Normal indigenous intestinal flora. In Hentges, D. J. (ed.), Human intestinal microflora in health and disease. London: Academic Press. pp. 3–31.Google Scholar
Fite, A., Macfarlane, G. T., Cummings, J. H.et al. (2004). Identification and quantitation of mucosal and faecal desulfovibrios using real-time PCR. Gut, 53, 523–9CrossRefGoogle Scholar
Florin, T. H. J., Neale, G., Gibson, G. R., Christl, S. U. and Cummings, J. H. (1991). Metabolism of dietary sulphate: absorption and excretion in humans. Gut, 32, 766–73CrossRefGoogle ScholarPubMed
Fox, J. G., Dewhirst, F. E., Fraser, G. J.et al. (1994). Intracellular Campylobacter-like organism from ferrets and hamsters with proliferative bowel disease is a Desulfovibrio sp. J. Clin. Microbiol., 32, 1229–37Google ScholarPubMed
Gardiner, K. R., Halliday, M. I., Barclay, G. R.et al. (1996). Significance of systemic endotoxaemia in inflammatory bowel disease. Gut, 36, 897–901CrossRefGoogle Scholar
Gebhart, C. J., Barns, S. M., McOrist, S., Lin, G.-F. and Lawson, G. H. K. (1993). Ileal symbiont intracellularis, an obligate intracellular bacterium of porcine intestines showing a relationship to Desulfovibrio species. Int. J. Syst. Bacteriol., 43, 533–8CrossRefGoogle ScholarPubMed
Gibson, G. R. (1990). A review: physiology and ecology of the sulphate-reducing bacteria. J. Appl. Bacteriol., 69, 769–97CrossRefGoogle ScholarPubMed
Gibson, G. R., Cummings, J. H. and Macfarlane, G. T. (1988a). Competition for hydrogen between sulphate-reducing bacteria and methanogenic bacteria from the human large intestine. J. Appl. Bacteriol., 65, 241–7CrossRefGoogle Scholar
Gibson, G. R., Cummings, J. H. and Macfarlane, G. T. (1988b) Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulphate reduction and methanogenesis by mixed populations of human gut bacteria. Appl. Environ. Microbiol., 54, 2750–5Google Scholar
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 Microbiol. Ecol., 86, 103–12CrossRefGoogle Scholar
Gibson, G. R., Cummings, J. H., Macfarlane, G. T.et al. (1990). Alternative pathways for hydrogen disposal during fermentation in the human colon. Gut, 31, 679–83CrossRefGoogle ScholarPubMed
Gibson, G. R. and Macfarlane, G. T. (1988). Chemostat enrichment of sulphate-reducing bacteria from the large gut. Lett. Appl. Microbiol., 7, 127–33CrossRefGoogle Scholar
Gibson, G. R., Macfarlane, G. T. and Cummings, J. H. (1988c). Occurrence of sulphate-reducing bacteria in human faeces and the relationship of dissimilatory sulphate reduction to methanogenesis in the large gut. J. Appl. Bacteriol., 65, 103–11CrossRefGoogle Scholar
Gibson, G. R., Macfarlane, S. and Macfarlane, G. T. (1993). Metabolic interactions involving sulphate-reducing and methanogenic bacteria in the human large intestine. FEMS Microbiol. Ecol., 12, 117–25CrossRefGoogle Scholar
Goldstein, E. J. C., Citron, D. M., Peraino, V. A. and Cross, S. A. (2003). Desulfovibrio desulfuricans bacteremia and review of human Desulfovibrio infections. J. Clin. Microbiol., 41, 2752–4CrossRefGoogle ScholarPubMed
Harmsen, H. J. M., Raangs, G. C., He, T., Degener, J. E. and Welling, G. W. (2002). Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl. Environ. Microbiol., 68, 2982–90CrossRefGoogle ScholarPubMed
Head, K. A. and Jurenka, J. S. (2003). Inflammatory bowel disease part 1: Ulcerative colitis – pathophysiology and coventional and alternative treatment options. Alt. Med. Rev., 8, 247–83Google Scholar
Hopkins, M. J., Macfarlane, G. T., Furrie, E., Fite, A. and Macfarlane, S. (2005). Characterisation of intestinal bacteria in infant stools using real-time PCR and northern hybridisation analyses. FEMS Microbiol. Ecol., 54, 77–85CrossRefGoogle ScholarPubMed
Hristova, K. R., Mau, M., Zheng, D.et al. (2000). Desulfotomaculum genus- and subgenus-specific 16S rRNA hybridization probes for environmental studies. Environ. Microbiol., 2, 143–59CrossRefGoogle ScholarPubMed
Huycke, M. M. and Gaskins, H. R. (2004). Commensal bacteria, redox stress, and colorectal cancer: mechanisms and models. Exp. Biol. Med., 229, 586–97CrossRefGoogle ScholarPubMed
Kirk, E. (1949). The quantity and composition of human colonic flatus. Gastroenterology, 12, 782–94Google ScholarPubMed
Kong, S. C., Furrie, E., Macfarlane, G. T. and Cummings, J. H. (2005). Regional variation of mRNA of hydrogen sulphide detoxification enzymes in the colon may predispose to ulcerative colitis. Gut, 54, Suppl. 2, 352.Google Scholar
Kong, S. C., Furrie, E., Madden, J.et al. (2004). Comparison of hydrogen sulphide detoxification enzyme mRNA expression in normal and ulcerative colitis rectal mucosae. Gut, 53, Suppl. 3, 142.Google Scholar
Leclerc, H., Oger, C., Beerens, H. and Mossel, D. A. (1979). Occurrence of sulphate-reducing bacteria in the human intestinal flora and in the water environment. Water Res., 14, 253–6CrossRefGoogle Scholar
Lepp, P. W., Brinig, M. M., Ouverney, C. C.et al. (2004). Methanogenic Archaea and human periodontal disease. Proc. Nat. Acad. Sci., 101, 6176–81CrossRefGoogle ScholarPubMed
Levitt, M. D. (1969). Production and excretion of hydrogen gas in man. New Eng. J. Med., 281, 122–7CrossRefGoogle ScholarPubMed
Levitt, M. D. (1971). Volume and composition of human intestinal gas determined by means of an intestinal washout technique. New Eng. J. Med., 284, 1394–8CrossRefGoogle Scholar
Levitt, M. D., Furne, J., Springfield, J., Suarez, F. and DeMaster, E. (1999). Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J. Clin. Invest., 104, 1107–14CrossRefGoogle ScholarPubMed
Levitt, M. D., Gibson, G. R. and Christl, S. U. (1995). Gas metabolism in the large intestine. In Gibson, G. R. and Macfarlane, G. T. (eds.), Human colonic bacteria: role in nutrition, physiology and health. Boca Raton, FL: CRC Press. pp. 131–54.Google Scholar
Loftus, E. V., Silverstein, M. D., Sandborn, W. J.et al. (2000). Ulcerative colitis in Olmsted County, Minnesota, 1940–1993: incidence, prevalence, and survival. Gut, 46, 336–43CrossRefGoogle Scholar
Loubinoux, J., Bisson-Boutelliez, C., Miller, N. and Faou, A. E. (2002). Isolation of the provisionally named Desulfovibrio fairfieldensis from human periodontal pockets. Oral Microbiol. Immunol., 17, 321–3CrossRefGoogle ScholarPubMed
Loubinoux, J., Bronowicji, J.-P., Pereira, I. A. C., Moungenel, J.-L. and Faou, A. E. (2002). Sulphate-reducing bacteria in human feces and their association with inflammatory diseases. FEMS Microbiol. Ecol., 40, 107–12CrossRefGoogle Scholar
Loubinoux, J., Jaulhac, B., Piemont, Y., Monteil, H. and Faou, A. E. (2003). Isolation of sulphate-reducing bacteria from human thoracoabdominal pus. J. Clin. Microbiol., 41, 1304–6CrossRefGoogle Scholar
Loubinoux, J., Mory, F., Pereira, I. A. C. and Faou, A. E. (2000). Bacteremia caused by a strain of Desulfovibrio related to the provisionally named Desulfovibrio fairfieldensis. J. Clin. Microbiol., 38, 931–4Google ScholarPubMed
Loubinoux, J., Valente, F. M. A., Pereira, A. C.et al. (2002). Reclassification of the only species of the genus Desulfomonas, Desulfomonas pigra, as Desulfovibrio piger comb. nov. Int. J. Syst. Evol. Microbiol., 52, 1305–8Google ScholarPubMed
Macfarlane, G. T., Gibson, G. R. and Cummings, J. H. (1992). Comparison of fermentation reactions in different regions of the human colon. J. Appl. Bacteriol., 72, 57–64Google ScholarPubMed
Macfarlane, G. T., Gibson, G. R. and Macfarlane, S. (1994). Short chain fatty acid and lactate production by human intestinal bacteria grown in batch and continuous culture. In Binder, H. J., Cummings, J. H. and Soergel, K. H. (eds.), Short chain fatty acids. Lancaster: Kluwer Academic Publishers. pp. 44–60.Google Scholar
Macfarlane, G. T. and McBain, A. J. (1999). The human colonic microbiota. In Gibson, G. R. and Roberfroid, M. (eds.), Colonic microflora, nutrition and health. London: Chapman & Hall. pp. 1–25.CrossRefGoogle Scholar
Macfarlane, S., Furrie, E., Cummings, J. H. and Macfarlane, G. T. (2004). Chemotaxonomic analysis of bacterial populations colonizing the rectal mucosa in patients with ulcerative colitis. Clin. Infect. Dis., 38, 1690–9CrossRefGoogle ScholarPubMed
Marcus, R., Marcus, A. J. and Watt, J. (1983). Chronic ulcerative disease of the colon in rabbits fed native carrageenans. Proc. Nutr. Soc., 42, 155A.Google Scholar
Marcus, R. and Watt, J. (1969). Seaweeds and ulcerative colitis in laboratory animals. Lancet, 2, 489–90CrossRefGoogle ScholarPubMed
Mayberry, J. F., Ballantyne, K. C., Hardcastle, J. D., Mangham, C. and Pye, G. (1989). Epidemiological study of asymptomatic inflammatory bowel disease: the identification of cases during a screening programme for colorectal cancer. Gut, 30, 481–3CrossRefGoogle ScholarPubMed
McDougall, R., Robson, J., Paterson, D. and Tee, W. (1997). Bacteremia caused by a recently described novel Desulfovibrio species. J. Clin. Microbiol., 35, 1805–8Google ScholarPubMed
Montgomery, S. M., Morris, D. L., Thompson, N. P.et al. (1998). Prevalence of inflammatory bowel disease in British 26 year olds: national longitudinal birth cohort. Brit. Med. J., 316, 1058–9CrossRefGoogle ScholarPubMed
Moore, JBabidge, W., Millard, S. and Roediger, W. E. W. (1998). Colonic luminal hydrogen sulfide is not elevated in ulcerative colitis. Dig. Dis. Sci., 43, 162–5CrossRefGoogle Scholar
Moore, W. E. C., Johnson, J. L. and Holdeman, L. V. (1976). Emendation of Bacteroidaceae and Butyrivibrio and descriptions of Desulfomonas gen. nov. and ten new species of the genera Desulfomonas, Butyrivibrio, Eubacterium, Clostridium and Ruminococcus. Int. J. Syst. Bact., 26, 238–52CrossRefGoogle Scholar
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. J. Appl. Microbiol., 85, 372–80CrossRefGoogle ScholarPubMed
Oghe, H., Furne, J. K., Springfield, J. et al. (2005). Association between fecal hydrogen sulfide production and pouchitis. Dis. Col. Rect., 48, 469–75Google Scholar
Pitcher, M. C. L. (1996). Sulphate-reducing bacteria, sulphur metabolism and ulcerative colitis. MD Thesis, University of Cambridge.
Pitcher, M. C. L., Beatty, E. R. and Cummings, J. H. (2000). The contribution of sulphate reducing bacteria and 5-aminosalicylic acid to faecal sulphide in patients with ulcerative colitis. Gut, 46, 64–72CrossRefGoogle ScholarPubMed
Pitcher, M. C. L., Beatty, E. R., Harris, R. M., Waring, R. H. and Cummings, J. H. (1998). Sulfur metabolism in ulcerative colitis. Investigation of detoxification enzymes in peripheral blood. Dig. Dis. Sci., 43, 2080–5CrossRefGoogle ScholarPubMed
Roediger, W. E. W., Duncan, A., Kapaniris, O. and Millard, S. (1993a). Sulphide impairment of substrate oxidation in rat colonocytes: a biochemical basis for ulcerative colitis?Clin. Sci., 85, 1–5CrossRefGoogle Scholar
Roediger, W. E. W., Duncan, A., Kapaniris, O. and Millard, S. (1993b). Reducing sulfur compounds of the colon impair colonocyte nutrition: implications for ulcerative colitis. Gastroenterology, 104, 802–9CrossRefGoogle Scholar
Roediger, W. E. W. and Nance, S. (1986). Metabolic induction of experimental ulcerative colitis by inhibition of fatty acid oxidation. Brit. J. Exp. Pathol., 67, 773–82Google ScholarPubMed
Rose, P., Moore, P. K., Ming, S. H.et al. (2005). Hydrogen sulphide protects colon cancer cells from chemopreventative agent β-phenylethyl isocyanate induced apotosis. World J. Gastroenterol., 11, 3990–7CrossRefGoogle Scholar
Salyers, A. A. and O'Brien, M. (1980). Cellular location of enzymes involved in chondroitin sulphate breakdown by Bacteroides thetaiotaomicron. J. Bacteriol., 143, 772–80Google ScholarPubMed
Stebbings, S., Munro, K., Simon, M. A.et al. (2002). Comparison of the faecal microflora of patients with ankylosing spondylitis and controls using molecular methods of analysis. Rheumatology, 41, 1395–401CrossRefGoogle ScholarPubMed
Stein, J., Schroder, O., Milovic, V. and Caspary, W. F. (1995). Mercaptopropionate inhibits butyrate uptake in isolated apical membrane vesicles of the rat distal colon. Gastroenterology, 108, 673–9CrossRefGoogle ScholarPubMed
Stephen, A. M. and Cummings, J. H. (1980). The microbial contribution to human faecal mass. J. Med. Microbiol., 13, 45–56CrossRefGoogle ScholarPubMed
Hoeven, J. S., Lieboom, C. W. A. and Schaeken, M. J. M. (1995). Sulphate-reducing bacteria in the periodontal pocket. Oral Microbiol. Immunol., 10, 288–90CrossRefGoogle Scholar
Watt, J. and Marcus, R. (1973). Experimental ulcerative disease of the colon in animals. Gut, 14, 506–10CrossRefGoogle Scholar
Zinkevich, V. and Beech, I. B. (2000). Screening of sulphate-reducing bacteria in colonoscopy samples from healthy and colitic gut mucosa. FEMS Microbiol. Ecol., 34, 147–55CrossRefGoogle Scholar

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
×