The TonB energy transduction systems in Vibrio species

Future Microbiology

Volumn 5, Issue 9, 2010, Pages 1403-1412

  Kuehl, Carole J ^a   Crosa, Jorge H ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

iron transport; outer membrane protein receptor; pathogenic Vibrio; proton motive force; siderophore; TonB protein; virulence

Indexed keywords

BACTERIAL PROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN TONB; PROTEIN TONB1; PROTEIN TONB2; SIDEROPHORE; TTPC PROTEIN; UNCLASSIFIED DRUG;

ALIIVIBRIO SALMONICIDA; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CYTOPLASM; ENERGY TRANSFER; ESCHERICHIA COLI; LISTONELLA ANGUILLARUM; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTON MOTIVE FORCE; REVIEW; VIBRIO; VIBRIO ALGINOLYTICUS; VIBRIO ANGUSTUM; VIBRIO CHOLERAE; VIBRIO CORALLIILTTICUS; VIBRIO FISCHERI; VIBRIO FURNISSII; VIBRIO HARVEYI; VIBRIO METSCHNIOVI; VIBRIO MIMICUS; VIBRIO ORIENTALIS; VIBRIO PARAHAEMOLYTICUS; VIBRIO SHILONII; VIBRIO SPLENDIDUS; VIBRIO VULNIFICUS;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; FISH DISEASES; HUMANS; IRON; MEMBRANE PROTEINS; MICE; PROTON-MOTIVE FORCE; SIDEROPHORES; VIBRIO; VIBRIO INFECTIONS; VIRULENCE;

VIBRIO;

EID: 77957562075     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.10.90     Document Type: Review

References (64)

1. Imlay JA: Cellular defenses against superoxide and hydrogen peroxide. Ann. Rev. Biochem. 77, 755-776 (2008).
2. Jordan A, Reichard P: Ribonucleotide reductases. Ann. Rev. Biochem. 67, 71-98 (1998).
3. Roux A, Payne SM, Gilmore MS: Microbial telesensing: probing the environment for friends, foes, and food. Cell Host Microbe 6(2), 115-124 (2009).
4. Hantke K: Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol. Gen. Genet. 182(2), 288-292 (1981).
5. Braun V: Energy-coupled transport and signal transduction through the gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor Proteins FEMS Microbiol. Rev. 16(4), 295-307 (1995).
6. Crosa JH, Mey AR, Payne SM: Iron Transport in Bacteria. ASM Press, DC, USA (2004).
7. Postle K, Larsen RA: TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20(3-4), 453-465 (2007).
8. Hantke K, Braun V: Membrane receptor dependent iron transport in Escherichia coli. FEBS Lett. 49(3), 301-305 (1975).
9. Fischer E, Gunter K, Braun V: Involvement of ExbB and TonB in transport across the outer membrane of Escherichia coli: phenotypic complementation of exb mutants by overexpressed tonB and physical stabilization of TonB by ExbB. J. Bacteriol. 171(9), 5127-5134 (1989).
10. Ahmer BM, Thomas MG, Larsen RA, Postle K: Characterization of the exbBD operon of Escherichia coli and the role of ExbB and ExbD in TonB function and stability. J. Bacteriol. 177(16), 4742-4747 (1995).
11. Hannavy K, Barr GC, Dorman CJ et al.: TonB protein of Salmonella typhimurium. A model for signal transduction between membranes. J. Mol. Biol. 216(4), 897-910 (1990).
12. Jaskula JC, Letain TE, Roof SK, Skare JT, Postle K: Role of the TonB amino terminus in energy transduction between membranes. J. Bacteriol. 176(8), 2326-2338 (1994).
13. Kampfenkel K, Braun V: Membrane topology of the Escherichia coli ExbD protein. J. Bacteriol. 174(16), 5485-5487 (1992).
14. Kampfenkel K, Braun V: Topology of the ExbB protein in the cytoplasmic membrane of Escherichia coli. J. Biol. Chem. 268(8), 6050-6057 (1993).
15. Karlsson M, Hannavy K, Higgins CF: A sequence-specific function for the N-terminal signal-like sequence of the TonB protein. Mol. Microbiol. 8(2), 379-388 (1993).
16. Ollis AA, Manning M, Held KG, Postle K: Cytoplasmic membrane protonmotive force energizes periplasmic interactions between ExbD and TonB. Mol. Microbiol. 73(3), 466-481 (2009).
17. Larsen RA, Letain TE, Postle K: In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli. Mol. Microbiol. 49(1), 211-218 (2003).
18. Letain TE, Postle K: TonB protein appears to transduce energy by shuttling between the cytoplasmic membrane and the outer membrane in Escherichia coli. Mol. Microbiol. 24(2), 271-283 (1997).
19. Chimento DP, Kadner RJ, Wiener MC: Comparative structural analysis of TonB-dependent outer membrane transporters: implications for the transport cycle. Proteins 59(2), 240-251 (2005).
20. Devanathan S, Postle K: Studies on colicin B translocation: FepA is gated by TonB. Mol. Microbiol. 65(2), 441-453 (2007).
21. Gumbart J, Wiener MC, Tajkhorshid E: Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys. J. 93(2), 496-504 (2007).
22. Ma L, Kaserer W, Annamalai R et al.: Evidence of ball-and-chain transport of ferric enterobactin through FepA. J. Biol. Chem. 282(1), 397-406 (2007).
23. Pawelek PD, Croteau N, Ng-Thow-Hing C et al.: Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312(5778), 1399-1402 (2006).
24. Shultis DD, Purdy MD, Banchs CN, Wiener MC: Outer membrane active transport: structure of the BtuB:TonB complex. Science 312(5778), 1396-1399 (2006).
25. Kim YR, Lee SE, Kim CM et al.: Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect. Immun. 71(10), 5461-5471 (2003).
26. Lee JH, Rho JB, Park KJ et al.: Role of flagellum and motility in pathogenesis of Vibrio vulnificus. Infect. Immun. 72(8), 4905-4910 (2004).
27. Stork M, Di Lorenzo M, Mourino S, Osorio CR, Lemos ML, Crosa JH: Two tonB systems function in iron transport in Vibrio anguillarum, but only one is essential for virulence. Infect. Immun. 72(12), 7326-7329 (2004).
28. Faruque SM, Biswas K, Udden SM et al.: Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl Acad. Sci. USA 103(16), 6350-6355 (2006).
29. Wyckoff EE, Mey AR, Payne SM: Iron acquisition in Vibrio cholerae. Biometals 20(3-4), 405-416 (2007).
30. Childers BM, Klose KE: Regulation of virulence in Vibrio cholerae: the ToxR regulon. Future Microbiol. 2, 335-344 (2007).
31. Occhino DA, Wyckoff EE, Henderson DP, Wrona TJ, Payne SM: Vibrio cholerae iron transport: haem transport genes are linked to one of two sets of tonB, exbB, exbD genes. Mol. Microbiol. 29(6), 1493-1507 (1998).
32. Seliger SS, Mey AR, Valle AM, Payne SM: The two TonB systems of Vibrio cholerae: redundant and specific functions. Mol. Microbiol. 39(3), 801-812 (2001).
33. OMalley SM, Mouton SL, Occhino DA et al.: Comparison of the heme iron utilization systems of pathogenic Vibrios. J. Bacteriol. 181(11), 3594-3598 (1999).
34. Wang Q, Liu Q, Cao X, Yang M, Zhang Y: Characterization of two TonB systems in marine fish pathogen Vibrio alginolyticus: their roles in iron utilization and virulence. Arch. Microbiol. 190(5), 595-603 (2008).
35. Litwin CM, Byrne BL: Cloning and characterization of an outer membrane protein of Vibrio vulnificus required for heme utilization: regulation of expression and determination of the gene sequence. Infect. Immun. 66(7), 3134-3141 (1998).
36. Wong HC, Liu CC, Yu CM, Lee YS: Utilization of iron sources and its possible roles in the pathogenesis of Vibrio parahaemolyticus. Microbiol Immunol. 40(11), 791-798 (1996).
37. Stork M, Otto BR, Crosa JH: A novel protein, TtpC, is a required component of the TonB2 complex for specific iron transport in the pathogens Vibrio anguillarum and Vibrio cholerae. J. Bacteriol. 189(5), 1803-1815 (2007).
38. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ: Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl Acad. Sci. USA 84(9), 2833-2837 (1987).
39. Larsen RA, Wood GE, Postle K: The conserved proline-rich motif is not essential for energy transduction by Escherichia coli TonB protein. Mol. Microbiol. 10(5), 943-953 (1993).
40. Stock JB, Rauch B, Roseman S: Periplasmic space in Salmonella typhimurium and Escherichia coli. J. Biol. Chem. 252(21), 7850-7861 (1977).
41. Mey AR, Payne SM: Analysis of residues determining specificity of Vibrio cholerae TonB1 for its receptors. J. Bacteriol. 185(4), 1195-1207 (2003).
42. Lopez CS, Peacock RS, Crosa JH, Vogel HJ: Molecular characterization of the TonB2 protein from the fish pathogen Vibrio anguillarum. Biochem. J. 418(1), 49-59 (2009).
43. Mey AR, Payne SM: Haem utilization in Vibrio cholerae involves multiple TonB-dependent haem receptors. Mol. Microbiol. 42(3), 835-849 (2001).
44. Kuehl CJ, Crosa JH: Molecular and genetic characterization of the TonB2-cluster TtpC protein in pathogenic vibrios. Biometals 22(1), 109-115 (2009).
45. Altschul SF, Madden TL, Schaffer AA et al.: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25(17), 3389-3402 (1997).
46. Alice AF, Naka H, Crosa JH: Global gene expression as a function of the iron status of the bacterial cell: influence of differentially expressed genes in the virulence of the human pathogen Vibrio vulnificus. Infect. Immun. 76(9), 4019-4037 (2008).
47. Di Lorenzo M, Poppelaars S, Stork M, Nagasawa M, Tolmasky ME, Crosa JH: A nonribosomal peptide synthetase with a novel domain organization is essential for siderophore biosynthesis in Vibrio anguillarum. J. Bacteriol. 186(21), 7327-7336 (2004).
48. Di Lorenzo M, Stork M, Naka H, Tolmasky ME, Crosa JH: Tandem heterocyclization domains in a nonribosomal peptide synthetase essential for siderophore biosynthesis in Vibrio anguillarum. Biometals 21(6), 635-648 (2008).
49. Actis LA, Potter SA, Crosa JH: Iron-regulated outer membrane protein OM2 of Vibrio anguillarum is encoded by virulence plasmid pJM1. J. Bacteriol. 161(2), 736-742 (1985).
50. Actis LA, Tolmasky ME, Farrell DH, Crosa JH: Genetic and molecular characterization of essential components of the Vibrio anguillarum plasmid-mediated iron-transport system. J. Biol. Chem. 263(6), 2853-2860 (1988).
51. Lopez CS, Crosa JH: Characterization of ferric-anguibactin transport in Vibrio anguillarum. Biometals 20(3-4), 393-403 (2007).
52. Nakamura S, Morimoto YV, Kami-ike N, Minamino T, Namba K: Role of a conserved prolyl residue (Pro173) of MotA in the mechanochemical reaction cycle of the proton-driven flagellar motor of Salmonella. J. Mol. Biol. 393(2), 300-307 (2009).
53. Berg HC: Bacterial flagellar motor. Curr. Biol. 18(16), R689-R691 (2008).
54. Jaques S, Kim YK, McCarter LL: Mutations conferring resistance to phenamil and amiloride, inhibitors of sodium-driven motility of Vibrio parahaemolyticus. Proc. Natl Acad. Sci. USA 96(10), 5740-5745 (1999).
55. Sato K, Homma M: Functional reconstitution of the Na+-driven polar flagellar motor component of Vibrio alginolyticus. J. Biol. Chem. 275(8), 5718-5722 (2000). (Pubitemid 30115213)
56. Sato K, Homma M: Multimeric structure of PomA, a component of the Na+-driven polar flagellar motor of Vibrio alginolyticus. J. Biol. Chem. 275(26), 20223-20228 (2000). (Pubitemid 30441635)
57. Zhai YF, Heijne W, Saier MHJ: Molecular modeling of the bacterial outer membrane receptor energizer, ExbBD/TonB, based on homology with the flagellar motor, MotAB. Biochim. Biophys. Acta 1614(2), 201-210 (2003).
58. Balado M, Osorio CR, Lemos ML: FvtA is the receptor for the siderophore vanchrobactin in Vibrio anguillarum: utility as a route of entry for vanchrobactin analogues. Appl. Environ. Microbiol. 75(9), 2775-2783 (2009).
59. Griffiths GL, Sigel SP, Payne SM, Neilands JB: Vibriobactin, a siderophore from Vibrio cholerae. J. Biol. Chem. 259(1), 383-385 (1984).
60. Yamamoto S, Okujo N, Fujita Y, Saito M, Yoshida T, Shinoda S: Structures of two polyamine-containing catecholate siderophores from Vibrio fluvialis. J. Biochem. 113(5), 538-544 (1993).
61. Webster AC, Litwin CM: Cloning and characterization of vuuA, a gene encoding the Vibrio vulnificus ferric vulnibactin receptor. Infect. Immun. 68(2), 526-534 (2000).
62. Biosca EG, Fouz B, Alcaide E, Amaro C: Siderophore-mediated iron acquisition mechanisms in Vibrio vulnificus biotype 2. Appl. Environ. Microbiol. 62(3), 928-935 (1996).
63. Tanabe T, Naka A, Aso H et al.: A novel aerobactin utilization cluster in Vibrio vulnificus with a gene involved in the transcription regulation of the iutA homologue. Microbiol. Immunol. 49(9), 823-834 (2005).
64. Funahashi T, Tanabe T, Shiuchi K, Nakao H, Yamamoto S: Identification and characterization of genes required for utilization of desferri-ferrichrome and aerobactin in Vibrio parahaemolyticus. Biol. Pharm. Bull. 32(3), 359-365 (2009).