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. 1991 Sep;173(17):5352–5358. doi: 10.1128/jb.173.17.5352-5358.1991

Distribution of compatible solutes in the halophilic methanogenic archaebacteria.

M C Lai 1, K R Sowers 1, D E Robertson 1, M F Roberts 1, R P Gunsalus 1
PMCID: PMC208245  PMID: 1909318

Abstract

Accumulation of compatible solutes, by uptake or de novo synthesis, enables bacteria to reduce the difference between osmotic potentials of the cell cytoplasm and the extracellular environment. To examine this process in the halophilic and halotolerant methanogenic archaebacteria, 14 strains were tested for the accumulation of compatible solutes in response to growth in various extracellular concentrations of NaCl. In external NaCl concentrations of 0.7 to 3.4 M, the halophilic methanogens accumulated K+ ion and low-molecular-weight organic compounds. beta-Glutamate was detected in two halotolerant strains that grew below 1.5 M NaCl. Two unusual beta-amino acids, N epsilon-acetyl-beta-lysine and beta-glutamine (3-aminoglutaramic acid), as well as L-alpha-glutamate were compatible solutes among all of these strains. De novo synthesis of glycine betaine was also detected in several strains of moderately and extremely halophilic methanogens. The zwitterionic compounds (beta-glutamine, N epsilon-acetyl-beta-lysine, and glycine betaine) and potassium were the predominant compatible solutes among the moderately and extremely halophilic methanogens. This is the first report of beta-glutamine as a compatible solute and de novo biosynthesis of glycine betaine in the methanogenic archaebacteria.

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Selected References

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

  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. CHRISTIAN J. H., WALTHO J. A. Solute concentrations within cells of halophilic and non-halophilic bacteria. Biochim Biophys Acta. 1962 Dec 17;65:506–508. doi: 10.1016/0006-3002(62)90453-5. [DOI] [PubMed] [Google Scholar]
  3. Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ferguson T. J., Mah R. A. Isolation and characterization of an h(2)-oxidizing thermophilic methanogen. Appl Environ Microbiol. 1983 Jan;45(1):265–274. doi: 10.1128/aem.45.1.265-274.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Griffith O. W. Beta-amino acids: mammalian metabolism and utility as alpha-amino acid analogues. Annu Rev Biochem. 1986;55:855–878. doi: 10.1146/annurev.bi.55.070186.004231. [DOI] [PubMed] [Google Scholar]
  6. Henrichs S. M., Cuhel R. Occurrence of beta-Aminoglutaric Acid in Marine Bacteria. Appl Environ Microbiol. 1985 Aug;50(2):543–545. doi: 10.1128/aem.50.2.543-545.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kiene R. P., Oremland R. S., Catena A., Miller L. G., Capone D. G. Metabolism of reduced methylated sulfur compounds in anaerobic sediments and by a pure culture of an estuarine methanogen. Appl Environ Microbiol. 1986 Nov;52(5):1037–1045. doi: 10.1128/aem.52.5.1037-1045.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Landfald B., Strøm A. R. Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol. 1986 Mar;165(3):849–855. doi: 10.1128/jb.165.3.849-855.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Le Rudulier D., Strom A. R., Dandekar A. M., Smith L. T., Valentine R. C. Molecular biology of osmoregulation. Science. 1984 Jun 8;224(4653):1064–1068. doi: 10.1126/science.224.4653.1064. [DOI] [PubMed] [Google Scholar]
  10. Matheson A. T., Sprott G. D., McDonald I. J., Tessier H. Some properties of an unidentified halophile: growth characteristics, internal salt concentration, and morphology. Can J Microbiol. 1976 Jun;22(6):780–786. doi: 10.1139/m76-114. [DOI] [PubMed] [Google Scholar]
  11. Mathrani I. M., Boone D. R. Isolation and characterization of a moderately halophilic methanogen from a solar saltern. Appl Environ Microbiol. 1985 Jul;50(1):140–143. doi: 10.1128/aem.50.1.140-143.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Measures J. C. Role of amino acids in osmoregulation of non-halophilic bacteria. Nature. 1975 Oct 2;257(5525):398–400. doi: 10.1038/257398a0. [DOI] [PubMed] [Google Scholar]
  13. Meikle A. J., Reed R. H., Gadd G. M. Osmotic adjustment and the accumulation of organic solutes in whole cells and protoplasts of Saccharomyces cerevisiae. J Gen Microbiol. 1988 Nov;134(11):3049–3060. doi: 10.1099/00221287-134-11-3049. [DOI] [PubMed] [Google Scholar]
  14. Paterek J. R., Smith P. H. Isolation and characterization of a halophilic methanogen from great salt lake. Appl Environ Microbiol. 1985 Oct;50(4):877–881. doi: 10.1128/aem.50.4.877-881.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Roberts M. F., Choi B. S., Robertson D. E., Lesage S. Free amino acid turnover in methanogens measured by 15N NMR spectroscopy. J Biol Chem. 1990 Oct 25;265(30):18207–18212. [PubMed] [Google Scholar]
  16. Robertson D. E., Lesage S., Roberts M. F. Beta-aminoglutaric acid is a major soluble component of Methanococcus thermolithotrophicus. Biochim Biophys Acta. 1989 Sep 15;992(3):320–326. doi: 10.1016/0304-4165(89)90091-3. [DOI] [PubMed] [Google Scholar]
  17. Robertson D. E., Noll D., Roberts M. F., Menaia J. A., Boone D. R. Detection of the osmoregulator betaine in methanogens. Appl Environ Microbiol. 1990 Feb;56(2):563–565. doi: 10.1128/aem.56.2.563-565.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Robertson D. E., Roberts M. F., Belay N., Stetter K. O., Boone D. R. Occurrence of beta-glutamate, a novel osmolyte, in marine methanogenic bacteria. Appl Environ Microbiol. 1990 May;56(5):1504–1508. doi: 10.1128/aem.56.5.1504-1508.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sowers K. R., Robertson D. E., Noll D., Gunsalus R. P., Roberts M. F. N epsilon-acetyl-beta-lysine: an osmolyte synthesized by methanogenic archaebacteria. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9083–9087. doi: 10.1073/pnas.87.23.9083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sprott G. D., Jarrell K. F. K+, Na+, and Mg2+ content and permeability of Methanospirillum hungatei and Methanobacterium thermoautotrophicum. Can J Microbiol. 1981 Apr;27(4):444–451. doi: 10.1139/m81-067. [DOI] [PubMed] [Google Scholar]
  21. Sprott G. D., Shaw K. M., Jarrell K. F. Ammonia/potassium exchange in methanogenic bacteria. J Biol Chem. 1984 Oct 25;259(20):12602–12608. [PubMed] [Google Scholar]
  22. Vreeland R. H. Mechanisms of halotolerance in microorganisms. Crit Rev Microbiol. 1987;14(4):311–356. doi: 10.3109/10408418709104443. [DOI] [PubMed] [Google Scholar]
  23. WOLIN E. A., WOLIN M. J., WOLFE R. S. FORMATION OF METHANE BY BACTERIAL EXTRACTS. J Biol Chem. 1963 Aug;238:2882–2886. [PubMed] [Google Scholar]
  24. Yancey P. H., Clark M. E., Hand S. C., Bowlus R. D., Somero G. N. Living with water stress: evolution of osmolyte systems. Science. 1982 Sep 24;217(4566):1214–1222. doi: 10.1126/science.7112124. [DOI] [PubMed] [Google Scholar]

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