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How to be moderately halophilic with broad salt tolerance: clues from the genome of Chromohalobacter salexigens

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Abstract

We analyzed the amino acid composition of different categories of proteins of the moderately halophilic bacterium Chromohalobacter salexigens, as deduced from its genome sequence. Comparison with non-halophilic representatives of the γ-Proteobacteria (Escherichia coli, Pseudomonas aeruginosa, Vibrio cholerae) shows only a slight excess of acidic residues in the cytoplasmic proteins, and no significant differences were found in the acidity of membrane-bound proteins. In contrast, a very pronounced difference in mean pI value was observed for the periplasmic binding proteins of the ABC transport systems of C. salexigens and the non-halophiles E. coli and P. aeruginosa. V. cholerae, which is adapted to life in brackish water, showed intermediate values. The findings suggest that there is a major difference between the proteins of the moderate halophile C. salexigens and non-halophilic bacteria in their periplasmic proteins, exemplified by the substrate binding proteins of transport systems. The highly acidic nature of these proteins may enable them to function at high salt concentrations. The evolution of highly salt-tolerant prokaryotes may have depended on an increase in acidity of the proteins located external to the cytoplasmic membrane, enabling effective transport of nutrients into the cell.

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References

  • Arahal, DR, García MT, Vargas C, Cánovas D, Nieto JJ, Ventosa A (2001) Chromohalobacter salexigens sp. nov., a moderately halophilic species that includes Halomonas elongata DSM 3043 and ATCC 33174. Int J Syst Evol Microbiol 51:1457–1462

    CAS  PubMed  Google Scholar 

  • Bageshwar UK, Premkumar L, Gokhman, I, Savchenko T, Sussman JL, Zamir A (2004) Natural protein engineering: a uniquely salt-tolerant, but not halophilic, α-type carbonic anhydrase from algae proliferating in low- to hyper-saline environments. Protein Eng Design Selection 17:191–200

    Article  CAS  Google Scholar 

  • Britton KL, Stillman TJ, Yip KSP, Forterre P, Engel PC, Rice DW (1998) Insights into the molecular basis of salt tolerance from the study of glutamate dehydrogenase from Halobacterium salinarum. J Biol Chem 273:9023–9030

    Article  CAS  PubMed  Google Scholar 

  • Cánovas, D, Vargas C, Csonka L, Ventosa A, Nieto JJ (1996) Osmoprotectants in Halomonas elongata: high-affinity betaine transport system and choline-betaine pathway. J Bacteriol 178:7221–7226

    PubMed  Google Scholar 

  • Cánovas D, Vargas C, Iglesias-Guerra F, Csonka LN, Rhodes D, Ventosa A, Nieto, JJ (1997) Isolation and characterization of salt-sensitive mutants of the moderate halophile Halomonas elongata and cloning of the ectoine synthesis genes. J Biol Chem 272:25794–25801

    Article  PubMed  Google Scholar 

  • Cánovas D, Vargas C, Calderón MI, Ventosa A, Nieto JJ (1998) Characterization of the genes for the biosynthesis of the compatible solute ectoine in the moderately halophilic bacterium Halomonas elongata DSM 3043. Syst Appl Microbiol 21:487–497

    PubMed  Google Scholar 

  • Dennis PP, Shimmin LC (1997) Evolutionary divergence and salinity-mediated selection in halophilic archaea. Microbiol Mol Biol Rev 61:90–104

    CAS  PubMed  Google Scholar 

  • Elcock AH, McCammon JA (1998) Electrostatic contribution to the stability of halophilic proteins. J Mol Biol 280:731–748

    Article  CAS  PubMed  Google Scholar 

  • Falkenberg P, Matheson AT, Rollin Cf (1976) The properties of ribosomal proteins from a moderate halophile. Biochim Biophys Acta 434:474–482

    CAS  PubMed  Google Scholar 

  • Falkenberg P, Yaguchi M, Roy C, Zuker M (1986) The primary structure of the ribosomal A-protein (L12) from the moderate halophile NRCC 41227. Biochem Cell Biol 64:675–680

    CAS  PubMed  Google Scholar 

  • Fischer M, Gokhman I, Pick U, Zamir A (1996) A salt-resistant plasma membrane carbonic anhydrase is induced by salt in Dunaliella salina. J Biol Chem 271:17718–17723

    Article  PubMed  Google Scholar 

  • Fischer M, Gokhman I, Pick U, Zamir A (1997) A structurally novel transferrin-like protein accumulates in the plasma membrane of the unicellular green alga Dunaliella salina. J Biol Chem 272:1565–1570

    Article  PubMed  Google Scholar 

  • Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:273–328

    CAS  Google Scholar 

  • Gandbhir M, Rashed I, Marlière P, Mutzel R (1995) Convergent evolution of amino acid usage in archaebacterial and eubacterial lineages adapted to high salt. Res Microbiol 146:113–120

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF, Kushner DJ, Anderson PJ (1983) Amino acid composition of proteins in halophilic phototrophic bacteria of the genus Ectothiorhodospira. Can J Microbiol 29:1675–1679

    CAS  Google Scholar 

  • Kushner DJ (1978) Life in high salt and solute concentrations: halophilic bacteria. In: Kushner DJ (ed) Microbial life in extreme environments. Academic, London, pp 317–368

    Google Scholar 

  • Lanyi JK (1974) Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol Rev 38:272–290

    CAS  PubMed  Google Scholar 

  • Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91–98

    Article  CAS  PubMed  Google Scholar 

  • Matheson AT, Yaguchi M, Nazar RN, Visentin LP, Willick GE (1978) The structure of ribosomes from moderate and extreme halophilic bacteria. In: Caplan SR, Ginzburg M (eds) Energetics and structure of halophilic microorganisms. Elsevier/North Holland Biomedical Press, Amsterdam, pp 481–500

    Google Scholar 

  • Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164

    Article  CAS  PubMed  Google Scholar 

  • Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, Shukla HD, Lasky SR, Baliga NS, Thorsson V, Sbrogna J, Swartzell S, Weir D, Hall J. Dahl TA, Welti R, Goo YA, Leithauser B, Keller K, Cruz R, Danson MJ, Hough DW, Maddocks DG, Jablonski PE, Krebs MP. Angevine CM, Dale H, Isenberger TA, Peck RF, Pohlschroder M, Spudich JL, Jong K-H, Alam M, Freitas T, Hou S, Daniels CJ, Dennis PP, Omer AD, Ebhardt H, Lowe TM, Liang P, Riley M, Hood L, DasSarma S (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci USA 97:12176–12181

    Article  CAS  PubMed  Google Scholar 

  • Oren A (1986) Intracellular salt concentrations of the anaerobic halophilic eubacteria Haloanaerobium praevalens and Halobacteroides halobius. Can J Microbiol 32:4–9

    CAS  Google Scholar 

  • Oren A (1995) Comment on “Convergent evolution of amino acid usage in archaebacterial and eubacterial lineages adapted to high salt”, by M Gandbhir et al (Res Microbiol 1995, 146, 113–120). Res Microbiol 146:805–806

    Article  CAS  PubMed  Google Scholar 

  • Oren A (2002) Halophilic microorganisms and their environments. Kluwer, Dordrecht

    Google Scholar 

  • Oren A, Heldal M, Norland, Galinski EA (2002) Intracellular ion and organic solute concentrations of the extremely halophilic Bacterium Salinibacter ruber. Extremophiles 6:491–498

    Article  CAS  PubMed  Google Scholar 

  • Reistad R (1970) On the composition and nature of the bulk protein of extremely halophilic bacteria. Arch Microbiol 71:353–360

    CAS  Google Scholar 

  • Tokunaga H, Mitsuo K, Kamekura M, Tokunaga M (2004) Major outer membrane proteins in moderately halophilic eubacteria of the genera Chromohalobacter and Halomonas. J Basic Microbiol 44:232–240

    Article  CAS  PubMed  Google Scholar 

  • Ventosa A., Gutierrez MC, Garcia MT, Ruiz-Berraquero F (1989) Classification of “ Chromobacterium marismortui” in a new genus, Chromohalobacter gen nov, as Chromohalobacter marismortui comb nov, nom rev. Int J Syst Bacteriol 39:382–386

    Google Scholar 

  • Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544

    CAS  PubMed  Google Scholar 

  • Wydro R, Kogut M, Kushner DJ (1975) Salt response of ribosomes of a moderately halophilic bacterium. FEBS Lett 60:210–215

    Article  CAS  PubMed  Google Scholar 

  • Wydro RM, Madira W, Hiramatsu T, Kogut M, Kushner DJ (1977) Salt-sensitive in vitro protein synthesis by a moderately halophilic bacterium. Nature 269:824–825

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Lily Mana for technical assistance.

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Correspondence to Aharon Oren.

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Communicated by W. D. Grant

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Oren, A., Larimer, F., Richardson, P. et al. How to be moderately halophilic with broad salt tolerance: clues from the genome of Chromohalobacter salexigens. Extremophiles 9, 275–279 (2005). https://doi.org/10.1007/s00792-005-0442-7

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