Catalytic properties of Staphylococcus aureus and Bacillus members of the secondary cation/proton antiporter-3 (Mrp) family are revealed by an optimized assay in an Escherichia coli host

Journal of Bacteriology

Volumn 189, Issue 8, 2007, Pages 3081-3090

  Swartz, Talia H ^a   Ito, Masahiro ^b   Ohira, Takayuki ^b   Natsui, Shinsuke ^b   Hicks, David B ^a   Krulwich, Terry A ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b TOYO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPORTER; BACTERIAL PROTEIN; CALCIUM ION; CATION PROTON ANTIPORTER 3; MAGNESIUM ION; POTASSIUM ION; PROTON; SODIUM ION; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS; BACILLUS PSEUDOFIRMUS; BACILLUS SUBTILIS; BACTERIAL MEMBRANE; ESCHERICHIA COLI; FLUORESCENCE; MEMBRANE POTENTIAL; MEMBRANE VESICLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTON SODIUM EXCHANGE; RESPIRATORY CHAIN; STAPHYLOCOCCUS AUREUS;

BACILLUS; BACTERIAL PROTEINS; ESCHERICHIA COLI; HYDROGEN; LITHIUM; MEMBRANE POTENTIALS; MEMBRANES; POTENTIOMETRY; SODIUM; SODIUM-HYDROGEN ANTIPORTER; STAPHYLOCOCCUS AUREUS; TRANSFORMATION, GENETIC;

BACILLUS (BACTERIUM); BACILLUS PSEUDOFIRMUS; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA; STAPHYLOCOCCUS AUREUS;

EID: 34247874630     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00021-07     Document Type: Article

References (69)

1. Ambudkar, S. V., G. W. Zlotnick, and B. P. Rosen. 1984. Calcium efflux from Escherichia coli. Evidence for two systems. J. Biol. Chem. 259:6142-6146.
2. Armstrong, J. M. 1964. The molar extinction coefficient of 2,6-dichlorophenol indophenol. Biochim. Biophys. Acta 86:194-197.
3. Bayer, A. S., P. McNamara, M. R. Yeaman, N. Lucindo, T. Jones, A. L. Cheung, H. G. Sahl, and R. A. Proctor. 2006. Transposon disruption of the complex I NADH oxidoreductase gene (snoD) in Staphylococcus aureus is associated with reduced susceptibility to the microbicidal activity of thrombin-induced platelet microbicidal protein 1. J. Bacteriol. 188:211-222.
4. + and adaptation to alkaline pH in the cyanobacterium Anabaena sp. PCC7120. Microbiology 151:1671-1682.
5. + redox poise in Streptomyces coelicolor A3(2). EMBO J. 22:4856-4865.
6. Busch, W., and M. H. Saier, Jr. 2002. The transporter classification (TC) system, 2002. Crit. Rev. Biochem. Mol. Biol. 37:287-337.
7. Edwards, J. C., M. S. Johnson, and B. L. Taylor. 2006. Differentiation between electron transport sensing and proton motive force sensing by the Aer and Tsr receptors for aerotaxis. Mol. Microbiol. 62:823-837.
8. Farrell, M. J., and S. E. Finkel. 2003. The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. J. Bacteriol. 185:7044-7452.
9. + antiporter of Escherichia coli. Biochemistry 41:609-617.
10. Georgellis, D., O. Kwon, and E. C. Lin. 2001. Quinones as the redox signal for the Arc two-component system of bacteria. Science 292:2314-2316.
11. + antiporter of Escherichia coli in the membrane and its functional and structural consequences. Biochemistry 40:3403-3412.
12. + antiporter gene of Escherichia coli. Proc. Natl. Acad. Sci. USA 84:2615-2619.
13. + ratio by Rex (YdiH) and oxidation of NADH by NADH dehydrogenase Ndh in Bacillus subtilis. J. Bacteriol. 188:7062-7071.
14. + antiporter system of alkalophilic Bacillus species strain C-125. Mol. Microbiol. 14:939-946.
15. Hatefi, Y., and D. L. Stiggall. 1978. Preparation and properties of succinate: ubiquinone oxidoreductase (complex II). Methods Enzymol. 53:21-27.
16. Hicks, D. B., R. J. Plass, and P. G. Quirk. 1991. Evidence for multiple terminal oxidases, including cytochrome d, in facultatively alkaliphilic Bacillus firmus OF4. J. Bacteriol. 173:5010-5016.
17. + antiporter from Staphylococcus aureus. J. Bacteriol. 180:6642- 6648.
18. + antiporter and insights into mechanism of action and regulation by pH. Nature 534:1197-1202.
19. + and in pH homeostasis. J. Bacteriol. 181:2394-2402.
20. + and alkali but not cholate resistance. J. Bacteriol. 182:5663-5670.
21. + antiporters of Bacillus exhibit characteristics that are unanticipated for completely secondary active transporters. FEBS Lett. 496:117-120.
22. vBP has a role in motility, chemotaxis, and pH homeostasis of an alkaliphilic Bacillus. Proc. Natl. Acad. Sci. USA 101:10566-10571.
23. + antiporter-deficient strains by the overexpressed gene. J. Biol. Chem. 268:11296-11303.
24. Ji, Y., B. Zhang, S. F. Van, Horn, P. Warren, G. Woodnutt, M. K. Burnham, and M. Rosenberg. 2001. Identification of critical staphylococcal genes using conditional phenotypes generated by antisense RNA. Science 293:2266-2269.
25. Kao, M. C., E. Nakamaru-Ogiso, A. Matsuno-Yagi, and T. Yagi. 2005. Characterization of the membrane domain subunit NuoK (ND4L) of the NADH-quinone oxidoreductase from Escherichia coli. Biochemistry. 44:9545-9554.
26. + antiporter activity in Escherichia coli. J. Biol. Chem. 263:10408-10414.
27. + antiporter and a molybdate transporter are essential for arsenite oxidation in Agrobacterium tumefaciens. J. Bacteriol. 188:1577-1584.
28. Kita, K., K. Konishi, and Y. Anraku. 1986. Purification and properties of two terminal oxidase complexes of Escherichia coli aerobic respiratory chain. Methods Enzymol. 126:94-113.
29. + antiporter of alkaliphilic Bacillus sp. Extremophiles 4:253-258.
30. Kobayashi, K., S. D. Ehrlich, A. Albertini, G. Amati, K. K. Andersen, M. Arnaud, K. Asai, S. Ashikaga, S. Aymerich, P. Bessieres, F. Boland, S. C. Brignell, S. Bron, K. Bunai, J. Chapuis, L. C. Christiansen, A. Danchin, M. Debarbouille, E. Dervyn, E. Deuerling, K. Devine, S. K. Devine, O. Dreesen, J. Errington, S. Fillinger, S. J. Foster, Y. Fujita, A. Galizzi, R. Gardan, C. Eschevins, T. Fukushima, K. Haga, C. R. Harwood, M. Hecker, D. Hosoya, M. F. Hullo, H. Kakeshita, D. Karamata, Y. Kasahara, F. Kawamura, K. Koga, P. Koski, R. Kuwana, D. Imamura, M. Ishimaru, S. Ishikawa, I. Ishio, D. Le Coq, A. Masson, C. Mauel, R. Meima, R. P. Mellado, A. Moir, S. Moriya, E. Nagakawa, H. Nanamiya, S. Nakai, P. Nygaard, M. Ogura, T. Ohanan, M. O'Reilly, M. O'Rourke, Z. Pragai, H. M. Pooley, G. Rapoport, J. P. Rawlins, L. A. Rivas, C. Rivolta, A. Sadaie, Y. Sadaie, M. Sarvas, T. Sato, H. H. Saxild, E. Scanlan, W. Schumann, J. F. Seegers, J. Sekiguchi, A. Sekowska, S. J. Seror, M. Simon, P. Stragier, R. Studer, H. Takamatsu, T. Tanaka, M. Takeuchi, H. B. Thomaides, V. Vagner, J. M. van Dijl, K. Watabe, A. Wipat, H. Yamamoto, M. Yamamoto, Y. Yamamoto, K. Yamane, K. Yata, K. Yoshida, H. Yoshikawa, U. Zuber, and N. Ogasawara. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100:4678-4683.
31. + antiporter gene which is important for pH homeostasis of alkaliphilic Bacillus sp. C-125. Biochim. Biophys. Acta 1409:171-175.
32. + antiporter, ShaA, is required for initiation of sporulation in Bacillus subtilis. J. Bacteriol. 182:898-904.
33. Kosono, S., K. Haga, R. Tomizawa, Y. Kajiyama, K. Hatano, S. Takeda, Y. Wakai, M. Hino, and T. Kudo. 2005. Characterization of a multigene-encoded sodium/hydrogen antiporter (Sha) from Pseudomonas aeruginosa: its involvement in pathogenesis. J. Bacteriol. 187:5242-5248.
34. + antiporter in Bacillus subtilis. Biochim. Biophys. Acta 1758:627-635.
35. Li, Q., L. Li, T. Rejtar, D. J. Lessner, B. L. Karger, and J. G. Ferry. 2006. Electron transport in the pathway of acetate conversion to methane in the marine archaeon Methanosarcina acetivorans. J. Bacteriol. 188:702-710.
36. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods 25:402-408.
37. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
38. Macnab, R. M., and A. M. Castle. 1987. A variable stoichiometry model for pH homeostasis in bacteria. Biophys. J. 52:637-647.
39. Malpica, R., B. Franco, C. Rodriguez, O. Kwon, and D. Georgellis. 2004. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc. Natl. Acad. Sci. USA 101:13318-13323.
40. Mathiesen, C., and C. Hägerhäll. 2002. Transmembrane topology of the NuoL, M and N subunits of NADH:quinone oxidoreductase and their homologues among membrane-bound hydrogenases and bona fide antiporters. Biochim. Biophys. Acta 1556:121-132.
41. Mathiesen, C., and C. Hägerhäll. 2003. The 'antiporter module' of respiratory chain complex 1 includes the MrpC/NuoK subunit-a revision of the modular evolution scheme. FEBS Lett. 5459:7-13.
42. Matsushita, K., T. Ohnishi, and H. R. Kaback. 1987. NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. Biochemistry 26:7732-7737.
43. + antiporter of Vibrio parahaemolyticus. Biochem. Biophys. Res. Commun. 222:774-779.
44. + antiporters. Biochim. Biophys. Acta 1505:144-157.
45. + antiporter. Biochim. Biophys. Acta 1658:2-13.
46. Padan, E., E. Bibi, M. Ito, and T. A. Krulwich. 2005. Alkaline pH homeostasis in bacteria: new insights. Biochim. Biophys. Acta 1717:67-88.
47. + antiporter in Escherichia coli. J. Biol. Chem. 268:1729-1734.
48. + efflux system. Mol. Microbiol. 28:1091-1101.
49. Quirk, P. G., A. A. Guffanti, R. J. Plass, S. Clejan, and T. A. Krulwich. 1991. Protonophore-resistance and cytochrome expression in mutant strains of the facultative alkaliphile Bacillus firmus OF4. Biochim. Biophys. Acta 1058:131-140.
50. Radchenko, M. V., K. Tanaka, R. Waditee, S. Oshimi, Y. Matsuzaki, M. Fukuhara, H. Kobayashi, T. Takabe, and T. Nakamura. 2006. Potassium/proton antiport system of Escherichia coli. J. Biol. Chem. 281:19822- 19829.
51. + antiporter as well as the growth phenotype of Escherichia coli. J. Biol. Chem. 273:26470-26476.
52. Rosen, B. P. 1986. Ion extrusion systems in E. coli. Methods Enzymol. 125:328-386.
53. Safferling, M., H. Griffith, J. Jin, J. Sharp, M. De Jesus, C. Ng, T. A. Krulwich, and D. N. Wang. 2003. TetL tetracycline efflux protein from Bacillus subtilis is a dimer in the membrane and in detergent solution. Biochemistry 42:13969-13976.
54. Saier, M. H., Jr. 2000. Families of proteins forming transmembrane channels. J. Membr. Biol. 175:165-180.
55. Sturr, M. G., A. A. Guflanti, and T. A. Krulwich. 1994. Growth and bioenergetics of alkaliphilic Bacillus firmus OF4 in continuous culture at high pH. J. Bacteriol. 176:3111-3116.
56. Swartz, T. H., S. Ikewada, O. Ishikawa, M. Ito, and T. A. Krulwich. 2005. The Mrp system: a giant among monovalent cation/proton antiporters. Extremophiles 9:345-354.
57. + antiporter increases the activity of the malate:quinone oxidoreductase of an Escherichia coli respiratory mutant. J. Bacteriol. 187:388-391.
58. Swartz, T. H. 2006. Mrp systems of gram-positive bacteria: properties of the monovalent cation/proton antiport. Ph.D. dissertation. Mount Sinai School of Medicine of New York University, New York, NY.
59. Taglicht, D., E. Padan, and S. Schuldiner. 1993. Proton-sodium stoichiometry of NhaA, an electrogenic antiporter from Escherichia coli. J. Biol. Chem. 268:5382-5387.
60. Taylor, B. L., I. B. Zhulin, and M. S. Johnson. 1999. Aerotaxis and other energy-sensing behavior in bacteria. Annu. Rev. Microbiol. 53:103-128.
61. + antiporter of Escherichia coli. J. Biol. Chem. 279:3265-3272.
62. + exchangers (ycgO) perturbs cytoplasmic alkali cation balance at low osmolarity. Microbiology 147:3005-3013.
63. Vijaranakul, U., M. J. Nadakavukaren, D. O. Bayles, B. J. Wilkinson, and R. K. Jayaswal. 1997. Characterization of an NaCl-sensitive Staphylococcus aureus mutant and rescue of the NaCl-sensitive phenotype by glycine betaine but not by other compatible solutes. Appl. Environ. Microbiol. 63:1889-1897.
64. Waggoner, A. S. 1979. Dye indicators of membrane potential. Annu. Rev. Biophys. Bioeng. 8:47-68.
65. Wilkinson, B. J. 1997. Biology, p. 1-38. In K. B. Crossley and G. L. Archer (ed.), The staphylococci in human disease. Churchill Livingstone, London, United Kingdom.
66. Yagi, T. 1986. Purification and characterization of NADH dehydrogenase complex from Paracoccus denitrificans. Arch. Biochem. Biophys. 250:302-311.
67. + resistance and adaption to alkaline pH in Sinorhizobium fredii RT19 encodes a monovalent cation/proton antiporter. FEMS Microbiol. Lett. 262:172-177.
68. Yumoto, I. 2002. Bioenergetics of alkaliphilic Bacillus spp. J. Biosci. Bioeng. 93:342-353.
69. Zhou, L., X. H. Lei, B. R. Bochner, and B. L. Wanner. 2003. Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems. J. Bacteriol. 185:4956-4972.