High-affinity transport of choline-O-sulfate and its use as a compatible solute in Bacillus subtilis

Applied and Environmental Microbiology

Volumn 65, Issue 2, 1999, Pages 560-568

  Nau Wagner, Gabriele ^a   Boch, Jens ^a,b   Le Good, J Ann ^a,c   Bremer, Erhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b WASHINGTON UNIVERSITY   (United States)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BETAINE; CARBON; CARNITINE; CHOLINE; CHOLINE DERIVATIVE; CHOLINE O SULFATE; GAMMA BUTYROBETAINE; NITROGEN; SODIUM CHLORIDE; SULFUR; TRIMETHYLAMMONIUM SALT DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; MUTATION; NONHUMAN; OSMOLALITY;

BACILLUS SUBTILIS; OPUA;

EID: 0033013656     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/aem.65.2.560-568.1999     Document Type: Article

References (72)

1. Alexander, M. 1977. Microbial transformation of sulfur, p. 350-367. In Introduction to soil microbiology. John Wiley & Sons, New York, N.Y.
2. Bellenger, N., P. Nissen, T. C. Wood, and I. H. Segel. 1968. Specificity and control of choline-O-sulfate transport in filamentous fungi. J. Bacteriol. 96:1574-1585.
3. Bernard, T., M. Jebbar, S. Himidi-Kabbab, J. Hamelin, and C. Blanco. 1993. Ectoine accumulation and osmotic regulation in Brevibacterium linens. J. Gen. Microbiol. 139:129-136.
4. Blomberg, A. 1997. Osmoresponsive proteins and functional assessment strategies in Saccharomyces cerevisiae. Electrophoresis 18:1429-1440.
5. Bach, J., B. Kempf, and E. Bremer. 1994. Osmoregulation in Bacillus subtilis: synthesis of the osmoprotectant glycine betaine from exogenously provided choline. J. Bacteriol. 176:5364-5371.
6. Boch, J., B. Kempf, R. Schmid, and E. Bremer. 1996. Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes. J. Bacteriol. 178:5121-5129.
7. Boos, W., and J. M. Lucht. 1996. Periplasmic binding protein-dependent ABC transporters, pp. 1175-1209. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, B. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, vol. 1. ASM Press, Washington, D.C.
8. Burg, M., E. Kwon, and D. Kültz. 1997. Regulation of gene expression by hypertonicity. Annu. Rev. Physiol. 59:437-455.
9. Cánovas, D., C. Vargas, L. N. Csonka, A. Ventosa, and J. J. Nieto. 1996. Osmoprotectants in Halomonas elongata: high-affinity betaine transport system and choline-betaine pathway. J. Bacteriol. 178:7221-7226.
10. Catalfomo, P., J. H. Block, G. H. Constantine, and P. W. Kirk. 1972. Choline sulfate (ester) in marine higher fungi. Mar. Chem. 1:157-162.
11. Csonka, L. N., and W. Epstein. 1996. Osmoregulation, p. 1210-1223. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, vol. 1. ASM Press, Washington, D.C.
12. Csonka, L. N., and A. D. Hanson. 1991. Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 45:569-606.
13. D'Souza-Ault, M. R., L. T. Smith, and G. M. Smith. 1993. Roles of N-acetylglutaminylglutamine amide and glycine betaine in adaptation of Pseudomonas aeniginosa to osmotic stress. Appl. Environ. Microbiol. 59: 473-478.
14. Fitzgerald, J. W., and P. C. Luschinski. 1977. Further studies on the formation of choline sulfate by bacteria. Can. J. Microbiol. 23:483-490.
15. Galinski, E. A., and H. G. Trüper. 1994. Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol. Rev. 15:95-108.
16. Glaasker, E., W. N. Konings, and B. Poolman. 1996. Glycine betaine fluxes in Lactobacillus plantarum during osmostasis and hyper- and hypo-osmotic shock. J. Biol. Chem. 271:10060-10065.
17. Gouesbet, G., A. Trautwetter, S. Bonnassie, L. F. Wu, and C. Blanco. 1996. Characterization of the Erwinia chrysanthemi osmoprotectant transporter gene ousA. J. Bacteriol. 178:447-455.
18. Gravel, R. A. 1976. Choline-O-sulphate utilization in Aspergillus nidulans. Genet. Res. 28:261-276.
19. Gutierrez, J. A., and L. N. Csonka. 1995. Isolation and characterization of adenylate kinase (adk) mutations in Salmonella typhimurium which block the ability of glycine betaine to function as an osmoprotectant. J. Bacteriol. 177:390-400.
20. Hanson, A. D., and D. A. Gage. 1991. Identification and determination by fast atom bombardment mass spectrometry of the compatible solute choline-O-sulfate in Limonium species and other halophytes. Aust. J. Plant Physiol. 18:317-327.
21. Hanson, A. D., B. Rathinasabapathi, B. Chamberlin, and D. A. Gage. 1991. Comparative physiological evidence that β-alanine betaine and choline-O-sulfate act as compatible osmolytes in halophytic Limonium species. Plant Physiol. (Rockville) 97:1199-1205.
22. Hanson, A. D., B. Rathinasabapathi, J. Rivoal, M. Burnet, M. O. Dillon, and D. A. Gage. 1994. Osmoprotective compounds in the plumbaginaccae: a natural experiment in metabolic engineering of stress tolerance. Proc. Natl. Acad. Sci. USA 91:306-310.
23. Harada, T. 1964. The formation of sulphatases by Pseudomonas aeruginosa. Biochim. Biophys. Acta 81:193-196.
24. Harada, T., and B. Spencer. 1960. Choline sulphate in fungi. J. Gen. Microbiol. 22:520-527.
25. Harwood, C. R., and A. R. Archibald. 1990. Growth, maintenance and general techniques, p. 1-26. In C. R. Harwood and S. M. Cutting (ed.), Molecular biological methods for Bacillus. John Wiley & Sons, Inc., Chichester, United Kingdom.
26. Ikawa, M., A. Chakrvarti, and R. F. Taylor. 1972. Occurrence of choline in Lactobacillus plantarum. Can. J. Microbiol. 18:1241-1245.
27. Jebbar, M., R. Talibart, K. Gloux, T. Bernard, and C. Blanco. 1992. Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics. J. Bacteriol. 174:5027-5035.
28. Jebbar, M., C. von Blohn, and E. Bremer. 1997. Ectoine functions as an osmoprotectant in Bacillus subtilis and is accumulated via the ABC-transport system OpuC. FEMS Microbiol. Lett. 154:325-330.
29. Jewell, J. B., and E. R. Kashket. 1991. Osmotically regulated transport of proline by Lactobacillus acidophilus IFO 3532. Appl. Environ. Microbiol. 57:2829-2833.
30. Kappes, R., and E. Bremer. 1998. Response of Bacillus subtilis to high osmolarity: uptake of carnitine, crotonobetaine and γ-butyrobetaine via the ABC transport system OpuC. Microbiology 144:83-90.
31. Kappes, R. M., B. Kempf, and E. Bremer. 1996. Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD. J. Bacteriol. 178:5071-5079.
32. Kappes, R. M., B. Kempf, S. Kneip, J. Boch, J. Gade, J. Meier-Wagner, and E. Bremer. Two evolutionarily closely related ABC-transporters mediate the uptake of choline for synthesis of the osmoprotectant glycine betaine in Bacillus subtilis. Mol. Microbiol., in press.
33. Kempf, B., and E. Bremer. 1995. OpuA, an osmotically regulated binding protein-dependent transport system for the osmoprotectant glycine betaine in Bacillus subtilis. J. Biol. Chem. 270:16701-16713.
34. Kempf, B., and E. Bremer. 1998. Uptake and synthesis of compatible solutes as microbial stress responses to high osmolality environments. Arch. Microbiol. 170:319-330.
35. Kempf, B., J. Gade, and E. Bremer. 1997. Lipoprotein from the osmorogulated ABC transport system OpuA of Bacillus subtilis: purification of the glycine betaine binding protein and characterization of a functional lipidless mutant. J. Bacteriol. 179:6213-6220.
36. Kempf, B., J. Gade, and E. Bremer. 1998. Unpublished data.
37. Kets, E. P. W., M. N. Groot, E. A. Gallinski, and J. A. M. De Bont. 1997. Choline and acetylcholine: novel cationic osmolytes in Lactobacillus plantarum. Appl. Microbiol. Biotechnol. 48:94-98.
38. Lamark, T., I. Kaasen, M. W. Eshoo, P. Falkenberg, J. McDougall, and A. R. Strøm. 1991. DNA sequence and analysis of the bet genes encoding the osmoregulatory choline-glycine betaine pathway of Escherichia coli. Mol. Microbiol. 5:1049-1064.
39. Le Rudulier, D., A. R. Strøm, A. M. Dandekar, L. T. Smith, and R. C. Valentine. 1984. Molecular biology of osmoregulation. Science 224:1064-1068.
40. Lisa, T. A., C. H. Casale, and C. E. Domenech. 1994. Cholinesterase, acid phosphatase, and phospholipase C of Pseudomonas aeruginosa under hyperosmotic conditions in a high-phosphate medium. Curr. Microbiol. 28:71-76.
41. Markham, P., G. D. Robson, B. W. Bainbridge, and A. P. Trinci. 1993. Choline: its role in the growth of filamentous fungi and the regulation of mycelial morphology. FEMS Microbiol. Rev. 10:287-300.
42. Martins, L., R. Huber, H. Huber, K. Stetter, M. Da Costa, and H. Santos. 1997. Organic solutes in hyperthermophilic Archaea. Appl. Environ. Microbiol. 63:896-902.
43. Marzluf, G. A. 1972. Genetic and metabolic control of sulfate metabolism in Neurospora crassa: a specific permease for choline-O-sulfate. Biochem. Genet. 7:219-233.
44. Mason, T., and G. Blunden. 1989. Quaternary ammonium and tertiary sulphonium compounds of algal origin as alleviators of osmotic stress. Bot. Mar. 32:313-316.
45. Miller, K. J., and J. M. Wood. 1996. Osmoadaptation by rhizosphere bacteria. Annu. Rev. Microbiol. 50:101-136.
46. Miura, G. A., and T.-M. Shih. 1984. Cholinergic constituents in plants: characterization and distribution of acetylcholine and choline. Physiol. Plant. 61:417-421.
47. Moses, S., C. von Blohn, E. Bakker, and E. Bremer. 1998. Unpublished data.
48. Nissen, P. 1968. Choline sulfate permease: transfer of information from bacteria to higher plants? Biochem. Biophys. Res. Commun. 32:696-703.
49. Nissen, P., and A. A. Benson. 1964. Active transport of choline sulfate bv barley roots. Plant Physiol. 39:586-589.
50. Østerås, M., E. Boncompagni, N. Vincent, M.-C. Poggi, and D. Le Rudulier. 1998. Presence of a gene encoding choline sulfatase in Sinorhizobium meliloti bet operon: choline-O-sulfate is metabolized into glycine betaine. Proc. Natl. Acad. Sci. USA 95:11394-11399.
51. Park, Y.-I., and J. E. Gander. 1998. Choline derivatives involved in osmotolerance of Penicillium fellutanum. Appl. Environ. Microbiol. 64:273-278.
52. Peter, H., A. Burkovski, and R. Krämer. 1996. Isolation, characterization, and expression of the Corynebacterium glutamicum betP gene, encoding the transport system for the compatible solute glycine betaine. J. Bacteriol. 178:5229-5234.
53. Pollard, A., and R. G. Wyn Jones. 1979. Enzyme activities in concentrated solutions of glycine betaine and other solutes. Planta 144:291-298.
54. Poolman, B., and E. Glaasker. 1998. Regulation of compatible solute accumulation in bacteria. Mol. Microbiol. 29:397-407.
55. Pourkomailian, B., and I. R. Booth. 1994. Glycine betaine transport by Staphylococcus aureus: evidence for feedback regulation of the activity of the two transport systems. Microbiology 140:3131-3138.
56. Proctor, L. M., R. Lai, and R. P. Gunsalus. 1997. The methanogenic archaeon Methanosarcina thermophila TM-1 possesses a high-affinity glycine betaine transporter involved in osmotic adaptation. Appl. Environ. Microbiol. 63:2252-2257.
57. Record, M. T., Jr., E. S. Courtenay, D. S. Cayley, and H. J. Guttman. 1998. Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23:143-148.
58. Rhodes, D., and A. D. Hanson. 1993. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:357-384.
59. Rioval, J., and A. D. Hanson. 1994. Choline-O-sulfate biosynthesis in plants. Identification and partial characterization of a salinity-inducible choline sulfotransferase from species of Limonium (Plumbaginaceae). Plant Physiol. (Rockville) 106:1187-1193.
60. Robinson, P. M., and M. F. Roberts. 1997. Effects of osmolyte precursors on the distribution of compatible solutes in Methanohalophilus portucalensis. Appl. Environ. Microbiol. 63:4032-4038.
61. Rozwadowski, K. L., G. G. Khachatourians, and G. Selvaraj. 1991. Choline oxidase, a catabolic enzyme in Arthrobacter pascens, facilitates adaptation to osmotic stress in Escherichia coli. J. Bacteriol. 173:472-478.
62. Spencer, B., E. C. Hussey, B. A. Orsi, and J. M. Scott. 1968. Mechanism of choline-O-sulphate utilization in fungi. Biochem. J. 106:461-469.
63. Stevens, C. M., and P. Vohra. 1955. Occurrence of choline sulfate in Penicillium chrysogenum. J. Am. Chem. Soc. 77:4935-4936.
64. Stimeling, K. W., J. E. Graham, A. Kaenjak, and B. J. Wilkinson. 1994. Evidence for feedback (trans) regulation of, and two systems for, glycine betaine transport by Staphylococcus aureus. Microbiology 140:3139-3144.
65. Talibart, R., M. Jebbar, G. Gouesbet, S. Himdi-Kabbab, H. Wróblewski, C. Blanco, and T. Bernard. 1994. Osmoadaptation in rhizobia: ectoine-induced salt tolerance. J. Bacteriol. 176:5210-5217.
66. Tretyn, A., and R. E. Kendrick. 1991. Acetylcholine in plants: presence, metabolism and mechanism of action. Bot. Rev. 57:33-73.
67. Ventosa, A., J. J. Nieto, and A. Oren. 1998. Biology of moderately halophilic aerobic bacteria. Microbiol. Mol. Biol. Rev. 62:504-544.
68. Verheul, A., E. Glaasker, B. Poolman, and T. Abee. 1997. Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals. J. Bacteriol. 179:6979-6985.
69. von Blohn, C., B. Kempf, R. M. Kappes, and E. Bremer. 1997. Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B. Mol. Microbiol. 25:175-187.
70. Whatmore, A. M., J. A. Chudek, and R. H. Reed. 1990. The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. J. Gen. Microbiol. 136:2527-2535.
71. Xavier, K. B., L. O. Martins, R. Peist, M. Kossmaan, W. Boos, and H. Santos. 1996. High-affinity maltose/trehalose transport system in the hyperthermophilic archaeon Thermococcus litoralis. J. Bacteriol. 178:4773-4777.
72. Yancey, P. H. 1994. Compatible and counteracting solutes, p. 81-109. In K. Strange (ed.), Cellular and molecular physiology of cell volume regulation. CRC Press, Inc., Boca Raton, Fla.