1887

Abstract

Glycine betaine (GB) and its immediate precursors choline and carnitine, dimethylsulfonioacetate, dimethylsulfoniopropionate, ectoine and proline were effective osmoprotectants for , but pipecolate, trehalose and sucrose had no osmoprotective effect. GB was accumulated stably or transiently when succinate or glucose, respectively, was used as a carbon and energy source. The catabolite repression mediated by succinate occurred at both low and high salinities, and it did not involve the global regulators Vfr and Crc. A proteomic analysis showed that at least 21 proteins were induced when GB was used as a carbon and energy source, and provided evidence that succinate repressed the synthesis of all these proteins. Many of the proteins induced by GB (sarcosine oxidase, serine hydroxymethyltransferase and serine dehydratase) are involved in GB catabolism. In addition, GB uptake was stimulated at high medium osmolalities but it was insensitive to catabolite repression by succinate. Despite its ability to inhibit betaine catabolism, succinate did not allow any better growth of cells under hyperosmotic constraint. Conversely, as observed for cells supplied with glucose, a transient accumulation of GB was sufficient to provide a significant cell osmoprotection.

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2006-05-01
2019-10-21
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References

  1. Bernard, T., Jebbar, M., Rassouli, Y., Himdi-Kabbab, S., Hamelin, J. & Blanco, C. ( 1993; ). Ectoine accumulation and osmotic regulation in Brevibacterium linens. J Gen Microbiol 139, 129–138.[CrossRef]
    [Google Scholar]
  2. Berry, A., DeVault, J. D. & Chakrabarty, A. M. ( 1989; ). High osmolarity is a signal for enhanced algD transcription in mucoid and nonmucoid Pseudomonas aeruginosa strains. J Bacteriol 171, 2312–2317.
    [Google Scholar]
  3. Boncompagni, E., Dupont, L., Mignot, T., Østerås, M., Lambert, A., Poggi, M. C. & Le Rudulier, D. ( 2000; ). Characterization of a Sinorhizobium meliloti ATP-binding cassette histidine transporter also involved in betaine and proline uptake. J Bacteriol 182, 3717–3725.[CrossRef]
    [Google Scholar]
  4. Bremer, E. & Krämer, R. ( 2000; ). Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes in bacteria. In Bacterial Stress Responses, pp. 79–97. Edited by G. Storz & R. Hengge-Aronis. Washington, DC: American Society for Microbiology.
  5. Chlumsky, L. J., Zhang, L. & Jorns, M. S. ( 1995; ). Sequence analysis of sarcosine oxidase and nearby genes reveals homologies with key enzymes of folate one-carbon metabolism. J Biol Chem 270, 18252–18259.[CrossRef]
    [Google Scholar]
  6. Choquet, G., Jehan, N., Pissavin, C., Blanco, C. & Jebbar, M. ( 2005; ). OusB, a broad-specificity ABC-type transporter from Erwinia chrysanthemi, mediates uptake of glycine betaine and choline with a high affinity. Appl Environ Microbiol 71, 3389–3398.[CrossRef]
    [Google Scholar]
  7. Collier, D. N., Hager, P. W. & Phibbs, P. V., Jr ( 1996; ). Catabolite repression control in the Pseudomonads. Res Microbiol 147, 551–561.[CrossRef]
    [Google Scholar]
  8. Deretic, V., Govan, J. R., Konyecsni, W. M. & Martin, D. W. ( 1990; ). Mucoid Pseudomonas aeruginosa in cystic fibrosis: mutations in the muc loci affect transcription of the algR and algD genes in response to environmental stimuli. Mol Microbiol 4, 189–196.[CrossRef]
    [Google Scholar]
  9. D'Souza-Ault, M. R., Smith, L. T. & Smith, G. M. ( 1993; ). Roles of N-acetylglutaminylglutamine amide and glycine betaine in adaptation of Pseudomonas aeruginosa to osmotic stress. Appl Environ Microbiol 59, 473–478.
    [Google Scholar]
  10. Gouesbet, G., Jebbar, M., Talibart, R., Bernard, T. & Blanco, C. ( 1994; ). Pipecolic acid is an osmoprotectant for Escherichia coli taken up by the general osmoporters ProU and ProP. Microbiology 140, 2415–2422.[CrossRef]
    [Google Scholar]
  11. Gouffi, K., Bernard, T. & Blanco, C. ( 2000; ). Osmoprotection by pipecolic acid in Sinorhizobium meliloti: specific effects of d and l isomers. Appl Environ Microbiol 66, 2358–2364.[CrossRef]
    [Google Scholar]
  12. Holloway, B. W., Krishnapillai, V. & Morgan, A. F. ( 1979; ). Chromosomal genetics of Pseudomonas. Microbiol Rev 43, 73–102.
    [Google Scholar]
  13. Jebbar, M., Talibart, R., Gloux, K., Bernard, T. & Blanco, C. ( 1992; ). Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics. J Bacteriol 174, 5027–5035.
    [Google Scholar]
  14. Jebbar, M., von Blohn, C. & Bremer, E. ( 1997; ). Ectoine functions as an osmoprotectant in Bacillus subtilis and is accumulated via the ABC-transport system OpuC. FEMS Microbiol Lett 154, 325–330.[CrossRef]
    [Google Scholar]
  15. Jebbar, M., Sohn-Bosser, L., Bremer, E., Bernard, T. & Blanco, C. ( 2005; ). Ectoine-induced proteins in Sinorhizobium meliloti include an Ectoine ABC-type transporter involved in osmoprotection and ectoine catabolism. J Bacteriol 187, 1293–1304.[CrossRef]
    [Google Scholar]
  16. Kappes, R. M., Kempf, B. & Bremer, E. ( 1996; ). Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD. J Bacteriol 178, 5071–5079.
    [Google Scholar]
  17. Lucchesi, G. I., Lisa, T. A., Casale, C. H. & Domenech, C. E. ( 1995; ). Carnitine resembles choline in the induction of cholinesterase, acid phosphatase, and phospholipase C and in its action as an osmoprotectant in Pseudomonas aeruginosa. Curr Microbiol 30, 55–60.[CrossRef]
    [Google Scholar]
  18. Lucht, J. M. & Bremer, E. ( 1994; ). Adaptation of Escherichia coli to high osmolarity environments: osmoregulation of the high-affinity glycine betaine transport system ProU. FEMS Microbiol Rev 14, 3–20.[CrossRef]
    [Google Scholar]
  19. MacGregor, C. H., Arora, S. K., Hager, P. W., Dail, M. B. & Phibbs, P. V., Jr ( 1996; ). The nucleotide sequence of the Pseudomonas aeruginosa pyrE-crc-rph region and the purification of the crc gene product. J Bacteriol 178, 5627–5635.
    [Google Scholar]
  20. Massimelli, M. J., Beassoni, P. R., Forrellad, M. A., Barra, J. L., Garrido, M. N., Domenech, C. E. & Lisa, A. T. ( 2005; ). Identification, cloning, and expression of Pseudomonas aeruginosa phosphorylcholine phosphatase gene. Curr Microbiol 50, 251–256.[CrossRef]
    [Google Scholar]
  21. Meskys, R., Harris, R. J., Casaite, V., Basran, J. & Scrutton, N. S. ( 2001; ). Organization of the genes involved in dimethylglycine and sarcosine degradation in Arthrobacter spp. Implications for glycine betaine catabolism. Eur J Biochem 268, 3390–3398.[CrossRef]
    [Google Scholar]
  22. Miller, J. H. ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  23. Pichereau, V., Pocard, J.-A., Hamelin, J., Blanco, C. & Bernard, T. ( 1998; ). Differential effects of dimethylsulfoniopropionate, dimethylsulfonioacetate, and other S-methylated compounds on the growth of Sinorhizobium meliloti at low and high osmolarities. Appl Environ Microbiol 64, 1420–1429.
    [Google Scholar]
  24. Robert, H., Le Marrec, C., Blanco, C. & Jebbar, M. ( 2000; ). Glycine betaine, carnitine, and choline enhance salinity tolerance and prevent the accumulation of sodium to a level inhibiting growth of Tetragenococcus halophila. Appl Environ Microbiol 66, 509–517.[CrossRef]
    [Google Scholar]
  25. Roeßler, M. & Müller, V. ( 2001; ). Osmoadaptation in bacteria and archaea: common principles and differences. Environ Microbiol 3, 743–754.[CrossRef]
    [Google Scholar]
  26. Sage, A. E. & Vasil, M. L. ( 1997; ). Osmoprotectant-dependent expression of plcH, encoding the hemolytic phospholipase C, is subject to novel catabolite repression control in Pseudomonas aeruginosa PAO1. J Bacteriol 179, 4874–4881.
    [Google Scholar]
  27. Sage, A. E., Vasil, A. I. & Vasil, M. L. ( 1997; ). Molecular characterization of mutants affected in the osmoprotectant-dependent induction of phospholipase C in Pseudomonas aeruginosa PAO1. Mol Microbiol 23, 43–56.[CrossRef]
    [Google Scholar]
  28. Salvano, M. A., Lisa, T. A. & Domenech, C. E. ( 1989; ). Choline transport in Pseudomonas aeruginosa. Mol Cell Biochem 85, 81–89.
    [Google Scholar]
  29. Serra, A. L., Mariscotti, J. F., Barra, J. L., Lucchesi, G. I., Domenech, C. E. & Lisa, A. T. ( 2002; ). Glycine betaine transmethylase mutant of Pseudomonas aeruginosa. J Bacteriol 184, 4301–4303.[CrossRef]
    [Google Scholar]
  30. Shortridge, V. D., Lazdunski, A. & Vasil, M. L. ( 1992; ). Osmoprotectants and phosphate regulate expression of phospholipase C in Pseudomonas aeruginosa. Mol Microbiol 6, 863–871.[CrossRef]
    [Google Scholar]
  31. Sleator, R. D. & Hill, C. ( 2002; ). Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26, 49–71.[CrossRef]
    [Google Scholar]
  32. Smith, L. T., Pocard, J.-A., Bernard, T. & Le Rudulier, D. ( 1988; ). Osmotic control of glycine betaine biosynthesis and degradation in Rhizobium meliloti. J Bacteriol 170, 3142–3149.
    [Google Scholar]
  33. Sriramulu, D. D., Lünsdorf, H., Lam, J. S. & Römling, U. ( 2005; ). Microcolony formation: a novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. J Med Microbiol 54, 667–676.[CrossRef]
    [Google Scholar]
  34. Stover, C. K., Pham, X. Q., Erwin, A. L. & 28 other authors ( 2000; ). Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406, 959–964.[CrossRef]
    [Google Scholar]
  35. Suh, S. J., Runyen-Janecky, L. J., Maleniak, T. C., Hager, P., MacGregor, C. H., Zielinski-Mozny, N. A., Phibbs, P. V., Jr & West, S. E. ( 2002; ). Effect of vfr mutation on global gene expression and catabolite repression control of Pseudomonas aeruginosa. Microbiology 148, 1561–1569.
    [Google Scholar]
  36. Talibart, R., Jebbar, M., Gouffi, K., Pichereau, V., Gouesbet, G., Blanco, C., Bernard, T. & Pocard, J. A. ( 1997; ). Transient accumulation of glycine betaine and dynamics of endogenous osmolytes in salt-stressed cultures of Sinorhizobium meliloti. Appl Environ Microbiol 63, 4657–4663.
    [Google Scholar]
  37. Wood, J. M., Bremer, E., Csonka, L. N., Krämer, R., Poolman, B., van der Heide, T. & Smith, L. T. ( 2001; ). Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 130, 437–460.[CrossRef]
    [Google Scholar]
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