Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1988 Nov;170(11):5298–5304. doi: 10.1128/jb.170.11.5298-5304.1988

Pathway and sites for energy conservation in the metabolism of glucose by Selenomonas ruminantium.

S B Melville 1, T A Michel 1, J M Macy 1
PMCID: PMC211604  PMID: 3141385

Abstract

On the basis of enzyme activities detected in extracts of Selenomonas ruminantium HD4 grown in glucose-limited continuous culture, at a slow (0.11 h-1) and a fast (0.52 h-1) dilution rate, a pathway of glucose catabolism to lactate, acetate, succinate, and propionate was constructed. Glucose was catabolized to phosphoenol pyruvate (PEP) via the Emden-Meyerhoff-Parnas pathway. PEP was converted to either pyruvate (via pyruvate kinase) or oxalacetate (via PEP carboxykinase). Pyruvate was reduced to L-lactate via a NAD-dependent lactate dehydrogenase or oxidatively decarboxylated to acetyl coenzyme A (acetyl-CoA) and CO2 by pyruvate:ferredoxin oxidoreductase. Acetyl-CoA was apparently converted in a single enzymatic step to acetate and CoA, with concomitant formation of 1 molecule of ATP; since acetyl-phosphate was not an intermediate, the enzyme catalyzing this reaction was identified as acetate thiokinase. Oxalacetate was converted to succinate via the activities of malate dehydrogenase, fumarase and a membrane-bound fumarate reductase. Succinate was then excreted or decarboxylated to propionate via a membrane-bound methylmalonyl-CoA decarboxylase. Pyruvate kinase was inhibited by Pi and activated by fructose 1,6-bisphosphate. PEP carboxykinase activity was found to be 0.054 mumol min-1 mg of protein-1 at a dilution rate of 0.11 h-1 but could not be detected in extracts of cells grown at a dilution rate of 0.52 h-1. Several potential sites for energy conservation exist in S. ruminantium HD4, including pyruvate kinase, acetate thiokinase, PEP carboxykinase, fumarate reductase, and methylmalonyl-CoA decarboxylase. Possession of these five sites for energy conservation may explain the high yields reported here (56 to 78 mg of cells [dry weight] mol of glucose-1) for S. ruminantium HD4 grown in glucose-limited continuous culture.

Full text

PDF
5303

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BRYANT M. P. The characteristics of strains of Selenomonas isolated from bovine rumen contents. J Bacteriol. 1956 Aug;72(2):162–167. doi: 10.1128/jb.72.2.162-167.1956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Caldwell D. R., Bryant M. P. Medium without rumen fluid for nonselective enumeration and isolation of rumen bacteria. Appl Microbiol. 1966 Sep;14(5):794–801. doi: 10.1128/am.14.5.794-801.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Collins L. B., Thomas T. D. Pyruvate kinase of Streptococcus lactis. J Bacteriol. 1974 Oct;120(1):52–58. doi: 10.1128/jb.120.1.52-58.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DENNIS D., KAPLAN N. O. LACTIC ACID RACEMIZATION IN CLOSTRIDIUM BUTYLICUM. Biochem Z. 1963;338:485–495. [PubMed] [Google Scholar]
  5. Dimroth P. Biotin-dependent decarboxylases as energy transducing systems. Ann N Y Acad Sci. 1985;447:72–85. doi: 10.1111/j.1749-6632.1985.tb18426.x. [DOI] [PubMed] [Google Scholar]
  6. Dimroth P. Characterization of a membrane-bound biotin-containing enzyme: oxaloacetate decarboxylase from Klebsiella aerogenes. Eur J Biochem. 1981 Apr;115(2):353–358. doi: 10.1111/j.1432-1033.1981.tb05245.x. [DOI] [PubMed] [Google Scholar]
  7. Hartree E. F. Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal Biochem. 1972 Aug;48(2):422–427. doi: 10.1016/0003-2697(72)90094-2. [DOI] [PubMed] [Google Scholar]
  8. Henderson C. The influence of extracellular hydrogen on the metabolism of Bacteroides ruminicola, Anaerovibrio lipolytica and Selenomonas ruminantium. J Gen Microbiol. 1980 Aug;119(2):485–491. doi: 10.1099/00221287-119-2-485. [DOI] [PubMed] [Google Scholar]
  9. Hilpert W., Dimroth P. Purification and characterization of a new sodium-transport decarboxylase. Methylmalonyl-CoA decarboxylase from Veillonella alcalescens. Eur J Biochem. 1983 May 16;132(3):579–587. doi: 10.1111/j.1432-1033.1983.tb07403.x. [DOI] [PubMed] [Google Scholar]
  10. Hilpert W., Schink B., Dimroth P. Life by a new decarboxylation-dependent energy conservation mechanism with Na as coupling ion. EMBO J. 1984 Aug;3(8):1665–1670. doi: 10.1002/j.1460-2075.1984.tb02030.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hobson P. N., Wallace R. J. Microbial ecology and activities in the rumen: Part II. Crit Rev Microbiol. 1982 May;9(4):253–320. doi: 10.3109/10408418209104492. [DOI] [PubMed] [Google Scholar]
  12. Isaacson H. R., Hinds F. C., Bryant M. P., Owens F. N. Efficiency of energy utilization by mixed rumen bacteria in continuous culture. J Dairy Sci. 1975 Nov;58(11):1645–1659. doi: 10.3168/jds.S0022-0302(75)84763-1. [DOI] [PubMed] [Google Scholar]
  13. Joyner A. E., Jr, Baldwin R. L. Enzymatic studies of pure cultures of rumen microorganisms. J Bacteriol. 1966 Nov;92(5):1321–1330. doi: 10.1128/jb.92.5.1321-1330.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kröger A., Dadák V., Klingenberg M., Diemer F. On the role of quinones in bacterial electron transport. Differential roles of ubiquinone and menaquinone in Proteus rettgeri. Eur J Biochem. 1971 Aug 16;21(3):322–333. doi: 10.1111/j.1432-1033.1971.tb01472.x. [DOI] [PubMed] [Google Scholar]
  15. Macy J., Kulla H., Gottschalk G. H2-dependent anaerobic growth of Escherichia coli on L-malate: succinate formation. J Bacteriol. 1976 Feb;125(2):423–428. doi: 10.1128/jb.125.2.423-428.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Melville S. B., Michel T. A., Macy J. M. Regulation of carbon flow in Selenomonas ruminantium grown in glucose-limited continuous culture. J Bacteriol. 1988 Nov;170(11):5305–5311. doi: 10.1128/jb.170.11.5305-5311.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Müller M. Biochemistry of protozoan microbodies: peroxisomes, alpha-glycerophosphate oxidase bodies, hydrogenosomes. Annu Rev Microbiol. 1975;29:467–483. doi: 10.1146/annurev.mi.29.100175.002343. [DOI] [PubMed] [Google Scholar]
  18. Otto R., Sonnenberg A. S., Veldkamp H., Konings W. N. Generation of an electrochemical proton gradient in Streptococcus cremoris by lactate efflux. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5502–5506. doi: 10.1073/pnas.77.9.5502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Paynter M. J., Elsden S. R. Mechanism of propionate formation by Selenomonas ruminantium, a rumen micro-organism. J Gen Microbiol. 1970 Apr;61(1):1–7. doi: 10.1099/00221287-61-1-1. [DOI] [PubMed] [Google Scholar]
  20. Relationship of lactate dehydrogenase specificity and growth rate to lactate metabolism by Selenomonas ruminantium. Appl Microbiol. 1975 Dec;30(6):916–921. doi: 10.1128/am.30.6.916-921.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Roggenkamp R., Reipen G., Hollenberg C. P. Mediation, by Saccharomyces cerevisiae translocation signals, of beta-lactamase transport through the Escherichia coli inner membrane and sensitive method for detection of signal sequences. J Bacteriol. 1986 Oct;168(1):467–469. doi: 10.1128/jb.168.1.467-469.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Russell J. B., Baldwin R. L. Comparison of maintenance energy expenditures and growth yields among several rumen bacteria grown on continuous culture. Appl Environ Microbiol. 1979 Mar;37(3):537–543. doi: 10.1128/aem.37.3.537-543.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Russell J. B., Baldwin R. L. Comparison of substrate affinities among several rumen bacteria: a possible determinant of rumen bacterial competition. Appl Environ Microbiol. 1979 Mar;37(3):531–536. doi: 10.1128/aem.37.3.531-536.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanwal B. D. Regulatory characteristics of the diphosphopyridine nucleotide-specific malic enzyme of Escherichia coli. J Biol Chem. 1970 Mar 10;245(5):1212–1216. [PubMed] [Google Scholar]
  25. Sanwal B. D., Smando R. Malic enzyme of Escherichia coli. Diversity of the effectors controlling enzyme activity. J Biol Chem. 1969 Apr 10;244(7):1817–1823. [PubMed] [Google Scholar]
  26. Steinmüller W., Bock E. Enzymatic studies on autotrophically, mixotrophically and heterotrophically grown Nitrobacter agilis with special reference to nitrite oxidase. Arch Microbiol. 1977 Oct 24;115(1):51–54. doi: 10.1007/BF00427844. [DOI] [PubMed] [Google Scholar]
  27. Stouthamer A. H., Bettenhaussen C. Utilization of energy for growth and maintenance in continuous and batch cultures of microorganisms. A reevaluation of the method for the determination of ATP production by measuring molar growth yields. Biochim Biophys Acta. 1973 Feb 12;301(1):53–70. doi: 10.1016/0304-4173(73)90012-8. [DOI] [PubMed] [Google Scholar]
  28. Tempest D. W., Neijssel O. M. The status of YATP and maintenance energy as biologically interpretable phenomena. Annu Rev Microbiol. 1984;38:459–486. doi: 10.1146/annurev.mi.38.100184.002331. [DOI] [PubMed] [Google Scholar]
  29. Ten Brink B., Konings W. N. Generation of an electrochemical proton gradient by lactate efflux in membrane vesicles of Escherichia coli. Eur J Biochem. 1980 Oct;111(1):59–66. doi: 10.1111/j.1432-1033.1980.tb06074.x. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Wallace R. J. Control of lactate production by Selenomonas ruminantium: homotropic activation of lactate dehydrogenase by pyruvate. J Gen Microbiol. 1978 Jul;107(1):45–52. doi: 10.1099/00221287-107-1-45. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES