PilB and PilT are ATPases acting antagonistically in type IV pilus function in Myxococcus xanthus

Journal of Bacteriology

Volumn 190, Issue 7, 2008, Pages 2411-2421

  Jakovljevic, Vladimir ^a   Leonardy, Simone ^a   Hoppert, Michael ^b   Søgaard Andersen, Lotte ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; PROTEIN PIL B; PROTEIN PIL T; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM PILUS; ENZYME ACTIVITY; GENETIC CONSERVATION; IN VITRO STUDY; IN VIVO STUDY; MUTAGENICITY; MYXOCOCCUS XANTHUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; STRUCTURE ANALYSIS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BLOTTING, WESTERN; FIMBRIAE, BACTERIAL; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; MYXOCOCCUS XANTHUS; OXIDOREDUCTASES; SEQUENCE HOMOLOGY, AMINO ACID;

MYXOCOCCUS XANTHUS;

EID: 41549119041     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01793-07     Document Type: Article

References (61)

1. Aukema, K. G., E. M. Kron, T. J. Herdendorf, and K. T. Forest. 2005. Functional dissection of a conserved motif within the pilus retraction protein PilT. J. Bacteriol. 187:611-618.
2. Camberg, J. L., T. L. Johnson, M. Patrick, J. Abendroth, W. G. Hol, and M. Sandkvist. 2007. Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids. EMBO J. 26:19-27.
3. Camberg, J. L., and M. Sandkvist. 2005. Molecular analysis of the Vibrio cholerae type II secretion ATPase EpsE. J. Bacteriol. 187:249-256.
4. Carbonnelle, E., S. Helaine, L. Prouvensier, X. Nassif, and V. Pelicic. 2005. Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fiber stability and function. Mol. Microbiol. 55:54-64.
5. Chen, Y., S.-J. Shiue, C.-W. Huang, J.-L. Chang, Y.-L. Chien, N.-T. Hu, and N.-L. Chan. 2005. Structure and function of the N-terminal domain, an essential component of the Xanthomonas campestris type II secretion system. J. Biol. Chem. 280:42356-42363.
6. Craig, L., M. E. Pique, and J. A. Tainer. 2004. Type IV pilus structure and bacterial pathogenecity. Nat. Rev. Microbiol. 2:363-378.
7. Craig, L., N. Volkmann, A. S. Arvai, M. E. Pique, M. Yeager, E. H. Egelman, and J. A. Tainer. 2006. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol. Cell 23:651-662.
8. Crowther, L. J., A. Yamagata, L. Craig, J. A. Tainer, and M. S. Donnenberg. 2005. The ATPase activity of BfpD is greatly enhanced by zinc and allosteric interactions with other Bfp proteins. J. Biol. Chem. 280:24839-24848.
9. Dubnau, D. 1999. DNA uptake in bacteria. Annu. Rev. Microbiol. 53:217-244.
10. Durand, E., A. Bernadac, G. Ball, A. Lazdunski, J. N. Sturgis, and A. Filloux. 2003. Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J. Bacteriol. 185:2749-2758.
11. Grana, D., T. Gardella, and M. M. Susskind. 1988. The effects of mutations in the ant promoter of phage P22 depend on context. Genetics 120:319-327.
12. Hare, S., R. Bayliss, C. Baron, and G. Waksman. 2006. A large domain swap inthe VirB11 ATPase of Brucella suis leaves the hexameric assembly intact. J. Mol. Biol. 360:56-66.
13. Herdendorf, T. J., D. R. McCaslin, and K. T. Forest. 2002. Aquifex aeolicus PilT, homologue of a surface motility protein, is a thermostable oligomeric NTPase. J. Bacteriol. 184:6465-6471.
14. Hodgkin, J., and D. Kaiser. 1977. Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc. Natl. Acad. Sci. USA 74:2938-2942.
15. Hodgkin, J., and D. Kaiser. 1979. Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol. Gen. Genet. 171:177-191.
16. Hu, N. T., W. M. Leu, M. S. Lee, A. Che, S. C. Cheng, Y. L. Song, and L. Y. Chen. 2002. XpsG, the major pseudopilin in Xanthomonas campestris pv campestris, forms a pilis-like structure between cytoplasmic and outer membrane. Biochem. J. 365:205-211.
17. Jelsbak, L., and D. Kaiser. 2005. Regulating pilin expression reveals a threshold for S motility in Myxococcus xanthus. J. Bacteriol. 187:2105-2112.
18. Jelsbak, L., and L. Søgaard-Andersen. 2002. Pattern formation by a cell surface-associated morphogen in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 99:2032-2037.
19. Kaiser, D. 2000. Bacterial motility: how do pili pull? Curr. Biol. 10:R777-780.
20. Kaiser, D. 1979. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 76:5952-5956.
21. Kashefi, K., and P. L. Hartzell. 1995. Genetic suppression and phenotypic masking of a Myxococcus xanthus frzF defect. Mol. Microbiol. 15:483-494.
22. Klausen, M., A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50:61-68.
23. Kruse, T., S. Lobedanz, N. M. S. Berthelsen, and L. Søgaard-Andersen. 2001. C-signal: a cell surface-associated morphogen that induces and coordinates multicellular fruiting body morphogenesis and sporulation in M. xanthus. Mol. Microbiol. 40:156-168.
24. Lanzer, M., and H. Bujard. 1988. Promoters largely determine the efficiency of repressor action. Proc. Natl. Acad. Sci. USA 85:8973-8977.
25. Lobedanz, S., and L. Søgaard-Andersen. 2003. Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev. 17:2151-2161.
26. Mahadevan, L., and P. Matsudaira. 2000. Motility powered by supramolecular springs and ratchets. Science 288:95-100.
27. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289-314.
28. Merz, A. J., and K. T. Forest. 2002. Bacterial surface motility: slime trails, grappling hooks and nozzles. Curr. Biol. 12:R297-R303.
29. Merz, A. J., M. So, and M. P. Sheetz. 2000. Pilus retraction powers bacterial twitching motility. Nature 407:98-102.
30. Mignot, T., J. P. Merlie, Jr., and D. R. Zusman. 2005. Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science 310:855-857.
31. Morand, P. C., E. Bille, S. Morelle, E. Eugène, J. L. Beretti, M. Wolfgang, T. F. Meyer, M. Koomey, and X. Nassif. 2004. Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J. 23:2009-2017.
32. Nakasugi, K., R. Alexova, C. J. Svenson, and B. A. Neilan. 2007. Functional analysis of PilT from the toxic cyanobacterium Microcystis aeruginosa PCC 7806. J. Bacteriol. 189:1689-1697.
33. Okamoto, S., and M. Ohmori. 2002. The cyanobacterial PilT protein responsible for cell motility and transformation hydrolyzes ATP. Plant Cell Physiol. 43:1127-1136.
34. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
35. Peabody, C. R., Y. J. Chung, M.-R. Yen, D. Vidal-Ingigliardi, A. P. Pugsley, and M. H. Saier, Jr. 2003. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051-3072.
36. Planet, P. J., S. C. Kachlany, R. DeSalle, and D. H. Figurski. 2001. Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. USA 98:2503-2508.
37. Possot, O., and A. P. Pugsley. 1994. Molecular characterization of PulE, a protein required for pullulanase secretion. Mol. Microbiol. 12:287-299.
38. Py, B., L. Loiseau, and F. Barras. 1999. Assembly of the type II secretion machinery of Erwinia chrysanthemi: direct interaction and associated conformational change between OutE, the putative ATP-binding component and the membrane component OutL. J. Mol. Biol. 289:659-670.
39. Rasmussen, A. A., S. Wegener-Feldbrügge, S. L. Porter, J. P. Armitage, and L. Søgaard-Andersen. 2006. Four signalling domains in the hybrid histidine protein kinase RodK of Myxococcus xanthus are required for activity. Mol. Microbiol. 60:525-534.
40. Robien, M. A., B. E. Krumm, M. Sandkvist, and W. G. Hol. 2003. Crystal structure of the extracellular protein secretion NTPase EpsE of Vibrio cholerae. J. Mol. Biol. 333:657-674.
41. Sakai, D., T. Horiuchi, and T. Komano. 2001. ATPase activity and multimer formation of PilQ protein are required for thin pilus biogenesis in plasmid R64. J. Biol. Chem. 276:17968-17975.
42. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Sandkvist, M., M. Bagdasarian, S. P. Howard, and V. J. DiRita. 1995. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. EMBO J. 14:1664-1673.
44. Satyshur, K. A., G. A. Worzalla, L. S. Meyer, E. K. Heiniger, K. G. Aukema, A. M. Misic, and K. T. Forest. 2007. Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility. Structure 15:363-376.
45. Sauvonnet, N., G. Vignon, A. P. Pugsley, and P. Gounon. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:2221-2228.
46. Savvides, S. N. 2007. Secretion superfamily ATPases swing big. Structure 15:255-257.
47. Savvides, S. N., H. J. Yeo, M. R. Beck, F. Blaesing, R. Lurz, E. Lanka, R. Buhrdorf, W. Fischer, R. Haas, and G. Waksman. 2003. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22:1969-1980.
48. Sexton, J. A., J. S. Pinkner, R. Roth, J. E. Heuser, S. J. Hultgren, and J. P. Vogel. 2004. The Legionella pneumophila PilT homologue DotB exhibits ATPase activity that is critical for intracellular growth. J. Bacteriol. 186:1658-1666.
49. Shi, W., and D. R. Zusman. 1993. The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc. Natl. Acad. Sci. USA 90:3378-3382.
50. Shiue, S.-J., K.-M. Kao, W.-M. Leu, L.-Y. Chen, N.-L. Chan, and N.-T. Hu. 2006. XpsE oligomerization triggered by ATP binding, not hydrolysis, leads to its association with XpsL. EMBO J. 25:1426-1435.
51. Skerker, J. M., and H. C. Berg. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA 98:6901-6904.
52. Sun, H., D. R. Zusman, and W. Shi. 2000. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 10:1143-1146.
53. Turner, L. R., J. C. Lara, D. N. Nunn, and S. Lory. 1993. Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 175:4962-4969.
54. Valentine, R. C., B. M. Shapiro, and E. R. Stadtman. 1968. Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry 7:2143-2152.
55. Wall, D., and D. Kaiser. 1999. Type IV pili and cell motility. Mol. Microbiol. 32:1-10.
56. Whitchurch, C. B., M. Hobbs, S. P. Livingston, V. Krishnapillai, and J. S. Mattick. 1991. Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubactcria. Gene 101:33-44.
57. White, D. J., R. Merod, B. Thomasson, and P. L. Hartzell. 2001. GidA is an FAD-binding protein involved in development of Myxococcus xanthus. Mol. Microbiol. 42:503-517.
58. Wu, S. S., and D. Kaiser. 1995. Genetic and functional evidence that type IV pili are required for social gliding motility in Myxococcus xanthus. Mol. Microbiol. 18:547-558.
59. Wu, S. S., J. Wu, and D. Kaiser. 1997. The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol. Microbiol. 23:109-121.
60. Yamagata, A., and J. A. Tainer. 2007. Hexameric structures of the archaeal secretion ATPase GspE and implications for a universal secretion mechanism. EMBO J. 26:878-890.
61. Yeo, H. J., S. N. Savvides, A. B. Herr, E. Lanka, and G. Waksman. 2000. Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol. Cell 6:1461-1472.