Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Sep;179(17):5471–5481. doi: 10.1128/jb.179.17.5471-5481.1997

Osmotically induced response in representatives of halophilic prokaryotes: the bacterium Halomonas elongata and the archaeon Haloferax volcanii.

F J Mojica 1, E Cisneros 1, C Ferrer 1, F Rodríguez-Valera 1, G Juez 1
PMCID: PMC179419  PMID: 9287003

Abstract

Haloferax volcanii and Halomonas elongata have been selected as representatives of halophilic Archaea and Bacteria, respectively, to analyze the responses to various osmolarities at the protein synthesis level. We have identified a set of high-salt-related proteins (39, 24, 20, and 15.5 kDa in H. elongata; 70, 68, 48, and 16 kDa in H. volcanii) whose synthesis rates increased with increasing salinities. A different set of proteins (60, 42, 15, and 6 kDa for H. elongata; 63, 44, 34, 18, 17, and 6 kDa for H. volcanii), some unique for low salinities, was induced under low-salt conditions. For both organisms, and especially for the haloarchaeon, adaptation to low-salt conditions involved a stronger and more specific response than adaptation to high-salt conditions, indicating that unique mechanisms may have evolved for low-salinity adaptation. In the case of H. volcanii, proteins with a typical transient response to osmotic shock, induced by both hypo- and hyperosmotic conditions, probably corresponding to described heat shock proteins and showing the characteristics of general stress proteins, have also been identified. Cell recovery after a shift to low salinities was immediate in both organisms. In contrast, adaptation to higher salinities in both cases involved a lag period during which growth and general protein synthesis were halted, although the high-salt-related proteins were induced rapidly. In H. volcanii, this lag period corresponded exactly to the time needed for cells to accumulate adequate intracellular potassium concentrations, while extrusion of potassium after the down-shift was immediate. Thus, reaching osmotic balance must be the main limiting factor for recovery of cell functions after the variation in salinity.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Bayley S. T., Morton R. A. Recent developments in the molecular biology of extremely halophilic bacteria. CRC Crit Rev Microbiol. 1978;6(2):151–205. doi: 10.3109/10408417809090622. [DOI] [PubMed] [Google Scholar]
  2. Brown A. D. Microbial water stress. Bacteriol Rev. 1976 Dec;40(4):803–846. doi: 10.1128/br.40.4.803-846.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Caplan A. J., Douglas M. G. Characterization of YDJ1: a yeast homologue of the bacterial dnaJ protein. J Cell Biol. 1991 Aug;114(4):609–621. doi: 10.1083/jcb.114.4.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Conway de Macario E., Macario A. J. Heat-shock response in Archaea. Trends Biotechnol. 1994 Dec;12(12):512–518. doi: 10.1016/0167-7799(94)90059-0. [DOI] [PubMed] [Google Scholar]
  6. Csonka L. N., Hanson A. D. Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol. 1991;45:569–606. doi: 10.1146/annurev.mi.45.100191.003033. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Culham D. E., Lasby B., Marangoni A. G., Milner J. L., Steer B. A., van Nues R. W., Wood J. M. Isolation and sequencing of Escherichia coli gene proP reveals unusual structural features of the osmoregulatory proline/betaine transporter, ProP. J Mol Biol. 1993 Jan 5;229(1):268–276. doi: 10.1006/jmbi.1993.1030. [DOI] [PubMed] [Google Scholar]
  9. Daniels C. J., McKee A. H., Doolittle W. F. Archaebacterial heat-shock proteins. EMBO J. 1984 Apr;3(4):745–749. doi: 10.1002/j.1460-2075.1984.tb01878.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ferrer C., Mojica F. J., Juez G., Rodríguez-Valera F. Differentially transcribed regions of Haloferax volcanii genome depending on the medium salinity. J Bacteriol. 1996 Jan;178(1):309–313. doi: 10.1128/jb.178.1.309-313.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gupta R. S., Singh B. Cloning of the HSP70 gene from Halobacterium marismortui: relatedness of archaebacterial HSP70 to its eubacterial homologs and a model for the evolution of the HSP70 gene. J Bacteriol. 1992 Jul;174(14):4594–4605. doi: 10.1128/jb.174.14.4594-4605.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gutierrez C., Devedjian J. C. Osmotic induction of gene osmC expression in Escherichia coli K12. J Mol Biol. 1991 Aug 20;220(4):959–973. doi: 10.1016/0022-2836(91)90366-e. [DOI] [PubMed] [Google Scholar]
  13. Hart D. J., Vreeland R. H. Changes in the hydrophobic-hydrophilic cell surface character of Halomonas elongata in response to NaCl. J Bacteriol. 1988 Jan;170(1):132–135. doi: 10.1128/jb.170.1.132-135.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  15. Lai M. C., Sowers K. R., Robertson D. E., Roberts M. F., Gunsalus R. P. Distribution of compatible solutes in the halophilic methanogenic archaebacteria. J Bacteriol. 1991 Sep;173(17):5352–5358. doi: 10.1128/jb.173.17.5352-5358.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Macario A. J., Dugan C. B., Clarens M., Conway de Macario E. dnaJ in Archaea. Nucleic Acids Res. 1993 Jun 11;21(11):2773–2773. doi: 10.1093/nar/21.11.2773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mellies J., Wise A., Villarejo M. Two different Escherichia coli proP promoters respond to osmotic and growth phase signals. J Bacteriol. 1995 Jan;177(1):144–151. doi: 10.1128/jb.177.1.144-151.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Miller V. L., Mekalanos J. J. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 1988 Jun;170(6):2575–2583. doi: 10.1128/jb.170.6.2575-2583.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mojica F. J., Juez G., Rodríguez-Valera F. Transcription at different salinities of Haloferax mediterranei sequences adjacent to partially modified PstI sites. Mol Microbiol. 1993 Aug;9(3):613–621. doi: 10.1111/j.1365-2958.1993.tb01721.x. [DOI] [PubMed] [Google Scholar]
  20. Mullakhanbhai M. F., Larsen H. Halobacterium volcanii spec. nov., a Dead Sea halobacterium with a moderate salt requirement. Arch Microbiol. 1975 Aug 28;104(3):207–214. doi: 10.1007/BF00447326. [DOI] [PubMed] [Google Scholar]
  21. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  22. Pérez-Fillol M., Rodríguez-Valera F. Potassium ion accumulation in cells of different halobacteria. Microbiologia. 1986 Oct;2(2):73–80. [PubMed] [Google Scholar]
  23. Ramirez R. M., Prince W. S., Bremer E., Villarejo M. In vitro reconstitution of osmoregulated expression of proU of Escherichia coli. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1153–1157. doi: 10.1073/pnas.86.4.1153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rodriguez-Valera F., Ruiz-Berraquero F., Ramos-Cormenzana A. Behaviour of mixed populations of halophilic bacteria in continuous cultures. Can J Microbiol. 1980 Nov;26(11):1259–1263. doi: 10.1139/m80-210. [DOI] [PubMed] [Google Scholar]
  25. Russell N. J., Kogut M. Haloadaptation: salt sensing and cell-envelope changes. Microbiol Sci. 1985 Nov;2(11):345–350. [PubMed] [Google Scholar]
  26. Vreeland R. H., Anderson R., Murray R. G. Cell wall and phospholipid composition and their contribution to the salt tolerance of Halomonas elongata. J Bacteriol. 1984 Dec;160(3):879–883. doi: 10.1128/jb.160.3.879-883.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vreeland R. H. Mechanisms of halotolerance in microorganisms. Crit Rev Microbiol. 1987;14(4):311–356. doi: 10.3109/10408418709104443. [DOI] [PubMed] [Google Scholar]
  28. Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yim H. H., Villarejo M. osmY, a new hyperosmotically inducible gene, encodes a periplasmic protein in Escherichia coli. J Bacteriol. 1992 Jun;174(11):3637–3644. doi: 10.1128/jb.174.11.3637-3644.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zhu J. K., Shi J., Bressan R. A., Hasegawa P. M. Expression of an Atriplex nummularia gene encoding a protein homologous to the bacterial molecular chaperone DnaJ. Plant Cell. 1993 Mar;5(3):341–349. doi: 10.1105/tpc.5.3.341. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES