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.
MeSH Terms
Animals
Cattle
Culture Media/metabolism
Enzyme Induction
Euryarchaeota/enzymology,growth & development,isolation & purification
Formates/metabolism
Hydrogen/metabolism
Male
Mercaptoethanol/analogs & derivatives
Mesna/biosynthesis
Rumen/microbiology
Substrate Specificity
Chemicals
Culture Media
Formates
Mercaptoethanol
Hydrogen
Mesna
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lovley D R
Greening R C
Ferry J G
References (27)
27 references, click to expand
-
Presence of growth factors for Methanobacterium ruminantium in both gram-positive and gram-negative bacteria.
Antonie Van Leeuwenhoek. 1974;40(4):585-9
PMID: 4219266
-
Factor 420-dependent pyridine nucleotide-linked formate metabolism of Methanobacterium ruminantium.
J Bacteriol. 1975 Jan;121(1):192-6
PMID: 234935
-
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):781-91
PMID: 827241
-
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):443-55
PMID: 541305
-
Metabolism of formate in Methanobacterium formicicum.
J Bacteriol. 1980 Jun;142(3):800-7
PMID: 6769911
-
Specific antisera and immunological procedures for characterization of methanogenic bacteria.
J Bacteriol. 1982 Jan;149(1):320-8
PMID: 6172417
-
Hydrogen-oxidizing methane bacteria. II. Electron microscopy.
J Bacteriol. 1968 Mar;95(3):1124-9
PMID: 5643051
-
Determination of concentration of hydrogen and some other cases dissolved in biological fluids.
Lab Pract. 1971 May;20(5):403-5 passim
PMID: 5104124
-
Features of rumen and sewage sludge strains of Eubacterium limosum, a methanol- and H2-CO2-utilizing species.
Appl Environ Microbiol. 1981 Jul;42(1):12-9
PMID: 6791591
-
Isolation and characterization of Methanobacterium ruminantium n. sp.
J Bacteriol. 1958 Jun;75(6):713-8
PMID: 13549377
-
Methanogens: reevaluation of a unique biological group.
Microbiol Rev. 1979 Jun;43(2):260-96
PMID: 390357
-
Characterization of Methanobacterium mobilis, sp. n., isolated from the bovine rumen.
J Bacteriol. 1968 May;95(5):1943-51
PMID: 4870286
-
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):402-12
PMID: 6889837
-
An analysis of the buffer system in the rumen of dairy cattle.
J Anim Sci. 1979 Dec;49(6):1536-44
PMID: 43325
-
Specificity and biological distribution of coenzyme M (2-mercaptoethanesulfonic acid).
J Bacteriol. 1979 Jan;137(1):256-63
PMID: 104960
-
Method for measuring dissolved hydrogen in anaerobic ecosystems: application to the rumen.
Appl Environ Microbiol. 1981 Feb;41(2):545-8
PMID: 7235697
-
Normal flora--rumen bacteria.
Am J Clin Nutr. 1970 Nov;23(11):1440-50
PMID: 4920104
-
Energy conservation in chemotrophic anaerobic bacteria.
Bacteriol Rev. 1977 Mar;41(1):100-80
PMID: 860983
-
Transport of coenzyme M (2-mercaptoethanesulfonic acid) in Methanobacterium ruminantium.
J Bacteriol. 1979 Jan;137(1):264-73
PMID: 33148
-
Effect of sampling location, time, and method of concentration of ammonia nitrogen in rumen fluid.
J Dairy Sci. 1976 Mar;59(3):459-64
PMID: 1262567
-
Pure culture studies of inhibitors for methanogenic bacteria.
Antonie Van Leeuwenhoek. 1972;38(3):281-7
PMID: 4538621
-
Formate as an intermediate in the bovine rumen fermentation.
J Bacteriol. 1970 May;102(2):389-97
PMID: 5419259
-
Amino acid concentrations in rumen fluid.
Appl Microbiol. 1967 Jan;15(1):148-51
PMID: 6031429
-
Secondary fermentation in the runen of a sheep given a diet based on molasses.
Br J Nutr. 1979 Mar;41(2):393-7
PMID: 427091
-
Association of methanogenic bacteria with ovine rumen ciliates.
Br J Nutr. 1982 Jan;47(1):95-9
PMID: 6800402
-
Kinetics of Formate Metabolism in Methanobacterium formicicum and Methanospirillum hungatei.
Appl Environ Microbiol. 1982 Sep;44(3):549-54
PMID: 16346087
-
Isolation of Methanobrevibacter smithii from human feces.
Appl Environ Microbiol. 1982 Jan;43(1):227-32
PMID: 6798932