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Gut microbiology – broad genetic diversity, yet specific metabolic niches

Published online by Cambridge University Press:  15 April 2008

R. John Wallace*
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
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Abstract

Analysis of 16S ribosomal RNA (rRNA)-encoding gene sequences from gut microbial ecosystems reveals bewildering genetic diversity. Some metabolic functions, such as glucose utilisation, are fairly widespread throughout the genetic spectrum. Others, however, are not. Despite so many phylotypes being present, single species or perhaps only two or three species often carry out key functions. Among ruminal bacteria, only three species can break down highly structured cellulose, despite the prevalence and importance of cellulose in ruminant diets, and one of those species, Fibrobacter succinogenes, is distantly related to the most abundant ruminal species. Fatty acid biohydrogenation in the rumen, particularly the final step of biohydrogenation of C18 fatty acids, stearate formation, is achieved only by a small sub-group of bacteria related to Butyrivibrio fibrisolvens. Individuals who lack Oxalobacter formigenes fail to metabolise oxalate and suffer kidney stones composed of calcium oxalate. Perhaps the most celebrated example of the difference a single species can make is the ‘mimosine story’ in ruminants. Mimosine is a toxic amino acid found in the leguminous plant, Leucaena leucocephala. Mimosine can cause thyroid problems by being converted to the goitrogen, 3-hydroxy-4(1H)-pyridone, in the rumen. Observations that mimosine-containing plants were toxic to ruminants in some countries but not others led to the discovery of Synergistes jonesii, which metabolises 3-hydroxy-4(1H)-pyridone and protects animals from toxicity. Thus, despite the complexities indicated by molecular microbial ecology and genomics, it should never be forgotten that gut communities contain important metabolic niches inhabited by species with highly specific metabolic capability.

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Copyright © The Animal Consortium 2008

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References

Akin, DE, Borneman, WS 1990. Role of rumen fungi in fibre degradation. Journal Dairy of Science 73, 30233032.CrossRefGoogle Scholar
Allison, MJ, Dawson, KA, Mayberry, WR, Foss, JG 1985. Oxalobacter formigenes gen.nov., sp.nov.: oxalate-degrading anaerobes from the gastrointestinal tract. Archives of Microbiology 141, 17.CrossRefGoogle ScholarPubMed
Allison, MJ, Mayberry, WR, McSweeney, CS, Stahl, DA 1992. Synergistes jonesii, gen. nov., sp. nov.: a rumen bacterium that degrades toxic pyridinediols. Systematic Applied Microbiology 15, 522529.CrossRefGoogle Scholar
Attwood, GT, Reilly, K, Patel, BKC 1996. Clostridium proteoclasticum sp. nov., a novel proteolytic bacterium from the bovine rumen. International Journal of Systematic Bacteriology 46, 753758.CrossRefGoogle Scholar
Banks, A, Hilditch, TP 1931. The glyceride structure of beef tallows. Biochemical Journal 25, 11681182.CrossRefGoogle ScholarPubMed
Chesson, A, Forsberg, CW 1997. Polysaccharide degradation by rumen microorganisms. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 329381. Chapman & Hall, London.CrossRefGoogle Scholar
Chin, SF, Storkson, J, Ha, YL, Pariza, MW 1992. Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognised class of anticarcinogens. Journal of Food Composition and Analysis 5, 185197.CrossRefGoogle Scholar
Coleman, GS 1985. The cellulase content of 15 species of entodiniomorphid protozoa, mixed bacteria and plant debris isolated from the ovine rumen. Journal of Agriculture Science 104, 349360.CrossRefGoogle Scholar
Coleman, GS 1986. The distribution of carboxymethylcellulase between fractions taken from the rumens of sheep containing no protozoa or one of five different protozoal populations. Journal of Agriculture Science 106, 121127.CrossRefGoogle Scholar
Costerton, JW, Damgaard, HN, Cheng, K-J 1974. Cell envelope morphology of rumen bacteria. Journal of Bacteriology 118, 11321143.CrossRefGoogle ScholarPubMed
Dawson, KA, Allison, MJ, Hartman, PA 1980. Isolation and some characteristics of anaerobic oxalate-degrading bacteria from the rumen. Applied and Environmental Microbiology 40, 833839.CrossRefGoogle ScholarPubMed
Devillard, E, Bera-Maillet, C, Flint, HJ, Scott, KP, Newbold, CJ, Wallace, RJ, Jouany, JP, Forano, E 2003. Characterization of XYN10B, a modular xylanase from the ruminal protozoan Polyplastron multivesiculatum, with a family 22 carbohydrate-binding module that binds to cellulose. Biochemical Journal 373, 495503.Google Scholar
Devillard, E, McIntosh, FM, Newbold, CJ, Wallace, RJ 2006. Rumen ciliate protozoa contain high concentrations of conjugated linoleic acids and vaccenic acid, yet do not hydrogenate linoleic acid or desaturate stearic acid. British Journal of Nutrition 96, 697704.Google ScholarPubMed
Duncan, SH, Richardson, AJ, Kaul, P, Holmes, RP, Allison, MJ, Stewart, CS 2002. Oxalobacter formigenes and its potential role in human health. Applied and environmental Microbiology 68, 38413847.CrossRefGoogle ScholarPubMed
Eckburg, PB, Bik, EM, Bernstein, CN, Purdom, E, Dethlefsen, L, Sargent, M, Gill, SR, Nelson, KE, Relman, DA 2005. Diversity of the human intestinal microbial flora. Science 308, 16351638.CrossRefGoogle ScholarPubMed
Edwards, JE, McEwan, NR, Travis, AJ, Wallace, RJ 2004. 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie Van Leeuwenhoek 86, 263281.CrossRefGoogle Scholar
Gordon, GLR, Phillips, MW 1993. Removal of anaerobic fungi from the rumen of sheep by chemical treatment and the effect on feed consumption and in vivo fibre digestion. Letters in Applied Microbiology 17, 220223.CrossRefGoogle Scholar
Harfoot, CG, Hazlewood, GP 1997. Lipid metabolism in the rumen. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 382426. Chapman & Hall, London.Google Scholar
Hayashi, H, Sakamoto, M, Benno, Y 2002. Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods. Microbiology and Immunology 46, 535548.CrossRefGoogle ScholarPubMed
Hegarty, MP, Court, RD, Christie, GS, Lee, CP 1976. Mimosine in Leucaena leucocephala is metabolised to a goitrogen in ruminants. Australian Veterinary Journal 52, 490.Google Scholar
Hegarty, MP, Lee, CP, Christie, GS, Court, RD, Haydock, KP 1979. The goitrogen 3-hydroxy-4(1H)-pyridone, a ruminal metabolite from Leucaena leucocephala: effects in mice and rats. Australian Journal of Biological Sciences 32, 2740.CrossRefGoogle ScholarPubMed
Hill, MJ 1983. Bile, bacteria and bowel cancer. Gut 24, 871875.CrossRefGoogle ScholarPubMed
Holmes, RP, Assimos, DG 1998. Glyoxylate synthesis, and its modulation and influence on oxalate synthesis. Journal of Urology 160, 16171624.CrossRefGoogle ScholarPubMed
Hooper, LV, Wong, MH, Thelin, A, Hansson, L, Falk, PG, Gordon, JI 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science 291, 881884.CrossRefGoogle ScholarPubMed
Hungate, RE 1966. The rumen and its microbes. Academic Press, New York and London.Google Scholar
Jones, R 1994. Management of anti-nutritive factors – with special reference to Leucaena. In Forage tree legumes in tropical agriculture (ed. RC Gutteridge and HM Shelton), p. 216. CAB Intemational, Wallingford, Oxon, UK.Google Scholar
Jones, RJ, Lowry, JB 1984. Australian goats detoxify the goitrogen 3-hydroxy-4(1H) pyridone (DHP) after rumen infusion from an Indonesian goat. Experientia 40, 14351436.CrossRefGoogle ScholarPubMed
Jones, RJ, Megarrity, RG 1986. Successful transfer of DHP-degrading bacteria from Hawaiian goats to Australian ruminals to overcome the toxicity of Leucaena. Australian Veterinary Journal 63, 259262.CrossRefGoogle ScholarPubMed
Kemp, P, White, RW, Lander, DJ 1975. The hydrogenation of unsaturated fatty acids by five bacterial isolates from the sheep rumen, including a new species. Journal of General Microbiology 90, 100114.CrossRefGoogle ScholarPubMed
Kritchevsky, D 2000. Antimutagenic and some other effects of conjugated linoleic acid. British Journal of Nutrition 83, 459465.CrossRefGoogle ScholarPubMed
Latham, MJ, Brooker, BE, Pethipher, GL, Harris, PJ 1978. Adhesion of Bacteroides succinogenes in pure culture and in the presence of Ruminococcus flavefaciens to cell walls in leaves of perennial ryegrass (Lolium perenne). Applied and Environmental Microbiology 35, 11661175.Google Scholar
Maia, MRG, Chaudhary, LC, Figueres, L, Wallace, RJ 2007. Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen. Antonie Van Leeuwenhoek 91, 303314.Google Scholar
McGavin, M, Lam, J, Forsberg, CW 1990. Regulation and distribution of Fibrobacter succinogenes subsp. succinogenes S85 endoglucanases. Applied and Environmental Microbiology 56, 12351244.CrossRefGoogle ScholarPubMed
Menotti, A, Kromhout, D, Blackburn, H, Fidanza, F, Buzina, R, Nissinen, A 1999. Food intake patterns and 25-year mortality from coronary heart disease: cross-cultural correlations in the Seven Countries Study. The Seven Countries Study Research Group. European Journal of Epidemiology 15, 507515.CrossRefGoogle Scholar
Mensink, RP 2005. Metabolic and health effects of isomeric fatty acids. Current Opinion in Lipidology 16, 2730.CrossRefGoogle ScholarPubMed
Miller, A, McGrath, E, Stanton, C, Devery, R 2003. Vaccenic acid (t11-18:1) is converted to c9,t11-CLA in MCF-7 and SW480 cancer cells. Lipids 38, 623632.Google Scholar
Neuhaus, TJ, Belzer, T, Blau, N, Hoppe, B, Sidhu, H, Leumann, E 2000. Urinary oxalate excretion in urolithiasis and nephrocalcinosis. Archives of Disease in Childhood 82, 322326.CrossRefGoogle ScholarPubMed
Paillard, D, McKain, N, Chaudhary, LC, Walker, ND, Pizette, F, Koppova, I, McEwan, NR, Kopecny, J, Vercoe, PE, Louis, P, Wallace, RJ 2006. Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen. Antonie Van Leeuwenhoek 91, 417422.CrossRefGoogle ScholarPubMed
Polan, CE, McNeill, JJ, Tove, SB 1964. Biohydrogenation of unsaturated fatty acids by rumen bacteria. Journal of Bacteriology 88, 10561064.CrossRefGoogle ScholarPubMed
Rincon, MT, Ding, SY, McCrae, SI, Martin, JC, Aurilia, V, Lamed, R, Shoham, Y, Bayer, EA, Flint, HJ 2003. Novel organization and divergent dockerin specificities in the cellulosome system of Ruminococcus flavefaciens. Journal of Bacteriology 185, 703713.Google Scholar
Savage, DC 2001. Microbial biota of the human intestine: a tribute to some pioneering scientists. Current Issues in Intestinal Microbiology 2, 115.Google ScholarPubMed
Schiffman, MH 1986. Epidemiology of fecal mutagenicity. Epidemiologic Reviews 8, 92105.CrossRefGoogle ScholarPubMed
Scollan, ND, Choi, NJ, Kurt, E, Fisher, AV, Enser, M, Wood, JD 2001. Manipulating the fatty acid composition of muscle and adipose tissue in beef cattle. British Journal Nutrition 85, 115124.CrossRefGoogle ScholarPubMed
Shelton, HM, Brewbaker, JL 1994. Leucaena leucocephala – the most widely used forage tree legume. In Forage tree legumes in tropical agriculture (ed. RC Gutteridge and HM Shelton). CAB Intemational, Wallingford, Oxon, UK.Google Scholar
Shorland, FB, Weenink, RO, Johns, AT 1955. Effect of the rumen on dietary fat. Nature 175, 11291130.Google Scholar
Sidhu, H, Allison, M, Peck, AB 1997. Identification and classification of Oxalobacter formigenes strains by using oligonucleotide probes and primers. Journal of Clinical Microbiology 35, 350353.CrossRefGoogle ScholarPubMed
Sidhu, H, Hoppe, B, Hesse, A, Tenbrock, K, Bromme, S, Rietschel, E, Peck, AB 1998. Absence of Oxalobacter formigenes in cystic fibrosis patients: a risk factor for hyperoxaluria. Lancet 352, 10261029.CrossRefGoogle ScholarPubMed
Stackebrandt, E, Ebers, J 2006. Taxonomic parameters revisited: tarnished gold standards. Microbiology Today 33, 152155.Google Scholar
Stewart, CS, Flint, HJ, Bryant, MP 1997. The rumen bacteria. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 1072. Chapman & Hall, London.CrossRefGoogle Scholar
Stewart, CS, Duncan, SH, Cave, DR 2004. Oxalobacter formigenes and its role in oxalate metabolism in the human gut. FEMS Microbiology Letters 230, 17.CrossRefGoogle ScholarPubMed
Suau, A, Bonnet, R, Sutren, M, Godon, JJ, Gibson, GR, Collins, MD, Dore, J 1999. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied and Environmental Microbiology 65, 47994807.CrossRefGoogle ScholarPubMed
Tajima, K, Aminov, RI, Nagamine, T, Ogata, K, Nakamura, M, Matsui, H, Benno, Y 1999. Rumen bacterial diversity as determined by sequence analysis of 16S rDNA libraries. FEMS Microbiology Ecology 29, 159169.CrossRefGoogle Scholar
Tajima, K, Arai, S, Ogata, K, Nagamine, T, Matsui, H, Nakamura, M, Aminov, RI, Benno, Y 2000. Rumen bacterial community transition during adaptation to high-grain diet. Anaerobe 6, 273284.Google Scholar
Tannock, GW, Munro, K, Harmsen, HJ, Welling, GW, Smart, J, Gopal, PK 2000. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Applied and Environmental Microbiology 66, 25782588.CrossRefGoogle ScholarPubMed
van de Vossenberg, JL, Joblin, KN 2003. Biohydrogenation of C18 unsaturated fatty acids to stearic acid by a strain of Butyrivibrio hungatei from the bovine rumen. Letters in Applied Microbiology 37, 424428.Google Scholar
Weisburg, WG, Barns, SM, Pelletier, DA, Lane, DJ 1991. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173, 697703.Google Scholar
Whigham, LD, Cook, ME, Atkinson, RL 2000. Conjugated linoleic acid: implications for human health. Pharmacological Research 42, 503510.Google Scholar
Whitford, MF, Forster, RJ, Beard, C, Gong, J, Teather, RM 1998. Phylogenetic analysis of rumen bacteria by comparative sequence analysis of cloned 16S rRNA genes. Anaerobe 4, 153163.Google Scholar
Zoetendal, EG, Akkermans, AD, De Vos, WM 1998. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Applied and Environmental Microbiology 64, 38543859.CrossRefGoogle ScholarPubMed