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. 1984 Jul;48(1):81–87. doi: 10.1128/aem.48.1.81-87.1984

Rapidly growing rumen methanogenic organism that synthesizes coenzyme M and has a high affinity for formate.

D R Lovley, R C Greening, J G Ferry
PMCID: PMC240316  PMID: 6433795

Abstract

Methanogenic bacteria with a coccobacillus morphology similar to Methanobrevibacter ruminantium were isolated from the bovine rumen. One isolate, 10-16B, represented a previously undescribed rumen population that, unlike M. ruminantium, synthesized coenzyme M, grew rapidly (mu = 0.24 h-1) on H2-CO2 in a complex medium, had simple nutritional requirements, and metabolized formate at reported rumen concentrations. H2 was metabolized to partial pressures 10-fold lower than those reported for the rumen. After H2 starvation for 26 h, strain 10-16B rapidly resumed growth when H2 was made available. The minimum concentrations of acetate (6 mM) and ammonia (less than 7 mM) that were required for optimal growth were lower than the reported acetate and ammonia concentrations in the rumen. Isoleucine and leucine stimulated growth, but only at concentrations (greater than 50 microM) higher than those reported for the rumen. Another coccobacillary methanogenic organism that synthesized coenzyme M was isolated from a different animal as were organisms that required an exogenous supply of coenzyme M. In general, methanogenic bacteria that required an exogenous supply of coenzyme M had lower maximum growth rates and more complex nutritional requirements than organisms that synthesized the cofactor. The ability of all isolates to metabolize formate below the detection limit of 10 microM indicated that, in contrast to previous reports, methanogenic bacteria have the potential to directly metabolize formate in the rumen. This study demonstrated that there are physiologically diverse populations of coccobacillary methanogenic bacteria in the rumen that can interact competitively and cooperatively.

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Selected References

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  1. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. Methanogens: reevaluation of a unique biological group. Microbiol Rev. 1979 Jun;43(2):260–296. doi: 10.1128/mr.43.2.260-296.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balch W. E., Wolfe R. S. New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressureized atmosphere. Appl Environ Microbiol. 1976 Dec;32(6):781–791. doi: 10.1128/aem.32.6.781-791.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Balch W. E., Wolfe R. S. Specificity and biological distribution of coenzyme M (2-mercaptoethanesulfonic acid). J Bacteriol. 1979 Jan;137(1):256–263. doi: 10.1128/jb.137.1.256-263.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Balch W. E., Wolfe R. S. Transport of coenzyme M (2-mercaptoethanesulfonic acid) in Methanobacterium ruminantium. J Bacteriol. 1979 Jan;137(1):264–273. doi: 10.1128/jb.137.1.264-273.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bryant M. P. Normal flora--rumen bacteria. Am J Clin Nutr. 1970 Nov;23(11):1440–1450. doi: 10.1093/ajcn/23.11.1440. [DOI] [PubMed] [Google Scholar]
  6. Conway de Macario E., Macario A. J., Wolin M. J. Specific antisera and immunological procedures for characterization of methanogenic bacteria. J Bacteriol. 1982 Jan;149(1):320–328. doi: 10.1128/jb.149.1.320-328.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Counotte G. H., van't Klooster A. T., van der Kuilen J., Prins R. A. An analysis of the buffer system in the rumen of dairy cattle. J Anim Sci. 1979 Dec;49(6):1536–1544. doi: 10.2527/jas1979.4961536x. [DOI] [PubMed] [Google Scholar]
  8. Czerkawski J. W., Breckenridge G. Determination of concentration of hydrogen and some other cases dissolved in biological fluids. Lab Pract. 1971 May;20(5):403–passim. [PubMed] [Google Scholar]
  9. Genthner B. R., Davis C. L., Bryant M. P. Features of rumen and sewage sludge strains of Eubacterium limosum, a methanol- and H2-CO2-utilizing species. Appl Environ Microbiol. 1981 Jul;42(1):12–19. doi: 10.1128/aem.42.1.12-19.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hungate R. E., Smith W., Bauchop T., Yu I., Rabinowitz J. C. Formate as an intermediate in the bovine rumen fermentation. J Bacteriol. 1970 May;102(2):389–397. doi: 10.1128/jb.102.2.389-397.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Langenberg K. F., Bryant M. P., Wolfe R. S. Hydrogen-oxidizing methane bacteria. II. Electron microscopy. J Bacteriol. 1968 Mar;95(3):1124–1129. doi: 10.1128/jb.95.3.1124-1129.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Leedle J. A., Bryant M. P., Hespell R. B. Diurnal variations in bacterial numbers and fluid parameters in ruminal contents of animals fed low- or high-forage diets. Appl Environ Microbiol. 1982 Aug;44(2):402–412. doi: 10.1128/aem.44.2.402-412.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Miller T. L., Wolin M. J., Conway de Macario E., Macario A. J. Isolation of Methanobrevibacter smithii from human feces. Appl Environ Microbiol. 1982 Jan;43(1):227–232. doi: 10.1128/aem.43.1.227-232.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Paynter M. J., Hungate R. E. Characterization of Methanobacterium mobilis, sp. n., isolated from the bovine rumen. J Bacteriol. 1968 May;95(5):1943–1951. doi: 10.1128/jb.95.5.1943-1951.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Prins R. A. Presence of growth factors for Methanobacterium ruminantium in both gram-positive and gram-negative bacteria. Antonie Van Leeuwenhoek. 1974;40(4):585–589. doi: 10.1007/BF00403822. [DOI] [PubMed] [Google Scholar]
  16. Prins R. A., van Nevel C. J., Demeyer D. I. Pure culture studies of inhibitors for methanogenic bacteria. Antonie Van Leeuwenhoek. 1972;38(3):281–287. doi: 10.1007/BF02328099. [DOI] [PubMed] [Google Scholar]
  17. Robinson J. A., Strayer R. F., Tiedje J. M. Method for measuring dissolved hydrogen in anaerobic ecosystems: application to the rumen. Appl Environ Microbiol. 1981 Feb;41(2):545–548. doi: 10.1128/aem.41.2.545-548.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rowe J. B., Loughnan M. L., Nolan J. V., Leng R. A. Secondary fermentation in the runen of a sheep given a diet based on molasses. Br J Nutr. 1979 Mar;41(2):393–397. doi: 10.1079/bjn19790048. [DOI] [PubMed] [Google Scholar]
  19. SMITH P. H., HUNGATE R. E. Isolation and characterization of Methanobacterium ruminantium n. sp. J Bacteriol. 1958 Jun;75(6):713–718. doi: 10.1128/jb.75.6.713-718.1958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Schauer N. L., Brown D. P., Ferry J. G. Kinetics of Formate Metabolism in Methanobacterium formicicum and Methanospirillum hungatei. Appl Environ Microbiol. 1982 Sep;44(3):549–554. doi: 10.1128/aem.44.3.549-554.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schauer N. L., Ferry J. G. Metabolism of formate in Methanobacterium formicicum. J Bacteriol. 1980 Jun;142(3):800–807. doi: 10.1128/jb.142.3.800-807.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stumm C. K., Gijzen H. J., Vogels G. D. Association of methanogenic bacteria with ovine rumen ciliates. Br J Nutr. 1982 Jan;47(1):95–99. doi: 10.1079/bjn19820013. [DOI] [PubMed] [Google Scholar]
  23. Thauer R. K., Jungermann K., Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977 Mar;41(1):100–180. doi: 10.1128/br.41.1.100-180.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tzing S. F., Bryant M. P., Wolfe R. S. Factor 420-dependent pyridine nucleotide-linked formate metabolism of Methanobacterium ruminantium. J Bacteriol. 1975 Jan;121(1):192–196. doi: 10.1128/jb.121.1.192-196.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wallace R. J. Effect of ammonia concentration on the composition, hydrolytic activity and nitrogen metabolism of the microbial flora of the rumen. J Appl Bacteriol. 1979 Dec;47(3):443–455. doi: 10.1111/j.1365-2672.1979.tb01205.x. [DOI] [PubMed] [Google Scholar]
  26. Wohlt J. E., Clark J. H., Blaisdell F. S. Effect of sampling location, time, and method of concentration of ammonia nitrogen in rumen fluid. J Dairy Sci. 1976 Mar;59(3):459–464. doi: 10.3168/jds.S0022-0302(76)84227-0. [DOI] [PubMed] [Google Scholar]
  27. Wright D. E., Hungate R. E. Amino acid concentrations in rumen fluid. Appl Microbiol. 1967 Jan;15(1):148–151. doi: 10.1128/am.15.1.148-151.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]

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