1887

Abstract

I-6 is a non-saccharolytic, amino-acid-fermenting anaerobe from the rumen, isolated by its ability to grow on pancreatic casein hydrolysate (PCH) as sole C source. This study investigated its metabolic properties and its likely ecological niche. Additional growth was supported by pyruvate, vinyl acetate, and, to a lesser extent, lactate and crotonate, and also by a mixture of amino acids (alanine, glycine, serine and threonine) predicted to be catabolized to pyruvate. No single amino acid supported growth, and peptides were required for growth on amino acids. Alanine, followed by leucine, serine and proline, were used most extensively during growth, but only alanine and asparate were extensively modified before incorporation. Growth on PCH, but not on pyruvate, was increased by the addition of acetate, propionate and butyrate. -Lactate was fermented incompletely, mainly to acetate, but no lactate-C was incorporated. Propionate and butyrate were utilized during growth, forming valerate and caproate, respectively. Labelling experiments suggested a metabolic pattern where two C atoms of butyrate, valerate and caproate were derived from amino acids, with the others being formed from acetate, propionate and butyrate. The metabolic strategy of therefore resembles that of , which ferments ethanol only when the reaction is coupled to acetate, propionate or butyrate utilization. The fermentative niche of appears to be to scavenge amino acids, lactate and possibly other metabolites in order to generate ATP via acetate formation, using volatile fatty acid elongation with C units derived from other substrates to dispose of reducing equivalents.

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2004-09-01
2024-03-28
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References

  1. Atasoglu C., Valdes C., Walker N. D., Newbold C. J., Wallace R. J. 1998; De novo synthesis of amino acids by the ruminal bacteriaPrevotella bryantiiB14, Selenomonas ruminantium HD4, and Streptococcus bovis ES1. Appl Environ Microbiol 64:2836–2843
    [Google Scholar]
  2. Attwood G. T., Klieve A. V., Ouwerkerk D., Patel B. K. C. 1998; Ammonia-hyperproducing bacteria from New Zealand ruminants. Appl Environ Microbiol 64:1796–1804
    [Google Scholar]
  3. Bartsch R. G., Barker H. A. 1961; A vinylacetate isomerase from Clostridium kluyveri. Arch Biochem Biophys 92:122–132 [CrossRef]
    [Google Scholar]
  4. Bauchop T., Elsden S. R. 1960; The growth of micro-organisms in relation to their energy supply. J Gen Microbiol 23:457–469 [CrossRef]
    [Google Scholar]
  5. Bidlingmeyer B. A., Cohen S. A., Tarvin T. L. 1984; Rapid analysis of amino acids using pre-column derivatisation. J Chromatogr 336:93–104 [CrossRef]
    [Google Scholar]
  6. Bornstein B. T., Barker H. A. 1948; The energy metabolism of Clostridium kluyveri and the synthesis of fatty acids. J Biol Chem 172:659–669
    [Google Scholar]
  7. Campbell I. M. 1974; Incorporation and dilution values – their calculation in mass spectrally assayed stable isotope labelling experiments. Bioorg Chem 3:386–397 [CrossRef]
    [Google Scholar]
  8. Cheeseman S. L., Hiom S. J., Weightman A. J., Wade W. G. 1996; Phylogeny of oral asaccharolytic eubacterium species determined by 16S ribosomal DNA sequence comparison and proposal of Eubacterium infirmum sp. nov. and Eubacterium tardum sp. nov. Int J Syst Bacteriol 46:957–959 [CrossRef]
    [Google Scholar]
  9. Chen G., Russell J. B. 1988; Fermentation of peptides and amino acids by a monensin-sensitive ruminal Peptostreptococcus. Appl Environ Microbiol 54:2742–2749
    [Google Scholar]
  10. Chen G., Russell J. B. 1989; More monensin-sensitive, ammonia-producing bacteria from the rumen. Appl Environ Microbiol 55:1052–1057
    [Google Scholar]
  11. Eschenlauer S. C. P., McKain N., Walker N. D., McEwan N. R., Newbold C. J., Wallace R. J. 2002; Ammonia production by ruminal microorganisms, and enumeration, isolation, and characterization of bacteria capable of growth on peptides and amino acids from the sheep rumen. Appl Environ Microbiol 68:4925–4931 [CrossRef]
    [Google Scholar]
  12. Goodall S. R., Byers F. M. 1978; Automated micro method for enzymatic l(+) and d(−) lactic acid determinations in biological fluid containing extracts. Anal Biochem 89:80–86 [CrossRef]
    [Google Scholar]
  13. Hamid M. A., Iwaku M., Hoshino E. 1994; The metabolism of phenylalanine and leucine by a cell suspension of Eubacterium brachy and the effects of metronidazole on metabolism. Arch Oral Biol 39:967–972 [CrossRef]
    [Google Scholar]
  14. Herbert D., Phipps P. J., Strange R. E. 1971; Chemical analysis of microbial cells. Methods Microbiol 5B209–344
    [Google Scholar]
  15. Hobson P. N. 1969; Rumen bacteria. Methods Microbiol 3B:133–139
    [Google Scholar]
  16. Leng R. A., Nolan J. V. 1984; Nitrogen metabolism in the rumen. J Dairy Sci 67:1072–1089 [CrossRef]
    [Google Scholar]
  17. Madan V. K., Hillmer P., Gottschalk G. 1973; Purification and properties of NADP-dependent l(+)-3-hydroxybutyryl-CoA dehydrogenase from Clostridium kluyveri. Eur J Biochem 32:51–56 [CrossRef]
    [Google Scholar]
  18. McSweeney C. S., Palmer B., Bunch R., Krause D. O. 1999; Isolation and characterization of proteolytic ruminal bacteria from sheep and goats fed the tannin-containing shrub legume Calliandra calothyrsus. Appl Environ Microbiol 65:3075–3083
    [Google Scholar]
  19. Paster B. J., Russell J. B., Yang C. M. J., Chow J. M., Woese C. R., Tanner R. 1993; Phylogeny of the ammonia-producing ruminal bacteria Peptostreptococcus anaerobius,Clostridium sticklandii and Clostridium aminophilum sp. nov. Int J Syst Bacteriol 43:107–110 [CrossRef]
    [Google Scholar]
  20. Richardson A. J., Calder A. G., Stewart C. S., Smith A. 1989; Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol 9:5–8 [CrossRef]
    [Google Scholar]
  21. Rooke J. A., Borman A. J., Armstrong D. G. 1990; The effect of inoculation with Lactobacillus plantarum on fermentation of herbage low in water soluble carbohydrate when ensiled in laboratory silos. Grass Forage Sci 45:143–152 [CrossRef]
    [Google Scholar]
  22. Russell J. B., Strobel H. J., Chen G. 1988; Enrichment and isolation of a ruminal bacterium with a very high specific activity of ammonia production. Appl Environ Microbiol 54:872–877
    [Google Scholar]
  23. Russell J. B., Onodera R., Hino T. 1991; Ruminal protein fermentation: new perspectives on previous contradictions. In Physiological Aspects of Digestion and Metabolism in Ruminants pp. 681–697 Edited by Tsuda T., Sasaki Y., Kawashima R. San Diego: Academic Press;
    [Google Scholar]
  24. Smith G. M., Kim B. W., Franke A. A., Roberts J. D. 1985; 13C NMR studies of butyric fermentation in Clostridium kluyveri. J Biol Chem 260:13509–13512
    [Google Scholar]
  25. Söhling B., Gottschalk G. 1996; Molecular analysis of the anaerobic succinate degradation pathway in Clostridium kluyveri. J Bacteriol 178:871–880
    [Google Scholar]
  26. Stewart C. S., Richardson A. J. 1989; Enhanced resistance of anaerobic rumen fungi to the ionophores monensin and lasalocid in the presence of methanogenic bacteria. J Appl Bacteriol 66:85–93 [CrossRef]
    [Google Scholar]
  27. Wade W. G., Downes J., Dymock D., Hiom S. J., Weightman A. J., Dewhirst F. E., Paster B. J., Tzellas N., Coleman B. 1999a; The family Coriobacteriaceae: reclassification of Eubacterium exiguum (Poco et al., 1996) and Peptostreptococcus heliotrinreducens (Lanigen 1976)as Slackia exigua gen. nov., comb. nov. and Slackia heliotrinireducens gen. nov., comb. nov., and Eubacterium lentum (Prevot 1938) as Eggerthella lenta gen. nov., comb. nov. Int J Syst Bacteriol 49:595–600 [CrossRef]
    [Google Scholar]
  28. Wade W. G., Downes J., Munson M. A., Weightman A. J. 1999b; Eubacterium minutum is an earlier synonym of Eubacterium tardum and has priority. Int J Syst Bacteriol 49:1939–1941 [CrossRef]
    [Google Scholar]
  29. Wallace R. J. 1978; Control of lactate production by Selenomonas ruminantium: homotropic activation of lactate dehydrogenase by pyruvate. J Gen Microbiol 107:45–52 [CrossRef]
    [Google Scholar]
  30. Wallace R. J., McKain N. 1990; A comparison of methods for determining the concentration of extracellular peptides in rumen fluid of sheep. J Agric Sci 114:101–105 [CrossRef]
    [Google Scholar]
  31. Wallace R. J., McKain N., McEwan N. R., Miyagawa E., Chaudhary L., King T. P., Walker N. D., Apajalahti J. H. A., Newbold C. J. 2003; Eubacterium pyruvativorans, a novel non-saccharolytic anaerobe from the rumen that ferments pyruvate and amino acids, forms caproate and utilises acetate and propionate. Int J Syst Evol Microbiol 53:965–970 [CrossRef]
    [Google Scholar]
  32. Williams A. G., Coleman G. S. 1997; The rumen protozoa. In The Rumen Microbial Ecosystem, 2nd edn. pp. 73–139 Edited by Hobson P. N., Stewart C. S. London: Chapman & Hall;
    [Google Scholar]
  33. Wolff R. A., Urben G. W. O'Herrin, M S., Kenealy W. R. 1993; Dehydrogenases involved in the conversion of succinate to 4-hydroxybutanoate by Clostridium kluyveri. Appl Environ Microbiol 59:1876–1882
    [Google Scholar]
  34. Wolin M. J., Miller T. L., Stewart C. S. 1997; Microbe–microbe interactions. In The Rumen Microbial Ecosystem, 2nd edn. pp. 467–491 Edited by Hobson P. N., Stewart C. S. London: Chapman & Hall;
    [Google Scholar]
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