Analysis of ATPases of putative secretion operons in the thermoacidophilic archaeon Free

Abstract

Gram-negative bacteria use a wide variety of complex mechanisms to secrete proteins across their membranes or to assemble secreted proteins into surface structures. As most archaea only possess a cytoplasmic membrane surrounded by a membrane-anchored S-layer, the organization of such complexes might be significantly different from that in Gram-negative bacteria. Five proteins of , SSO0120, SSO0572, SSO2316, SSO2387 and SSO2680, which are homologous to secretion ATPases of bacterial type II, type IV secretion systems and the type IV pili assembly machinery, were identified. The operon structures of these putative secretion systems encoding gene clusters and the expression patterns of the ATPases under different growth conditions were determined, and it was established that all five putative ATPases do show a divalent cation-dependent ATPase activity at high temperature. These results show that the archaeal secretion systems are related to the bacterial secretion systems and might be powered in a similar way.

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2005-03-01
2024-03-28
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References

  1. Albers S. V., Driessen A. M. 2002; Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus: a genomic survey. Arch Microbiol 177:209–216 [CrossRef]
    [Google Scholar]
  2. Albers S. V., Elferink M. G., Charlebois R. L., Sensen C. W., Driessen A. J., Konings W. N. 1999; Glucose transport in the extremely thermoacidophilic Sulfolobus solfataricus involves a high-affinity membrane-integrated binding protein. J Bacteriol 181:4285–4291
    [Google Scholar]
  3. Albers S. V., Driessen A. J, Szabó Z. 2003; Archaeal homolog of bacterial type IV prepilin signal peptidases with broad substrate specificity. J Bacteriol 185:3918–3925 [CrossRef]
    [Google Scholar]
  4. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [CrossRef]
    [Google Scholar]
  5. Bally M., Filloux A., Akrim M., Ball G., Lazdunski A., Tommassen J. 1992; Protein secretion in Pseudomonas aeruginosa – characterization of 7 Xcp genes and processing of secretory apparatus components by prepilin peptidase. Mol Microbiol 6:1121–1131 [CrossRef]
    [Google Scholar]
  6. Bardy S. L., Jarrell K. F. 2002; FlaK of the archaeon Methanococcus maripaludis possesses preflagellin peptidase activity. FEMS Microbiol Lett 208:53–59 [CrossRef]
    [Google Scholar]
  7. Bardy S. L., Jarrell K. F. 2003; Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae. Mol Microbiol 50:1339–1347 [CrossRef]
    [Google Scholar]
  8. Bardy S. L., Ng S. Y., Jarrell K. F. 2003; Prokaryotic motility structures. Microbiology 149:295–304 [CrossRef]
    [Google Scholar]
  9. Bhattacharjee M. K., Kachlany S. C., Fine D. H., Figurski D. H. 2001; Nonspecific adherence and fibril biogenesis by Actinobacillus actinomycetemcomitans: TadA protein is an ATPase. J Bacteriol 183:5927–5936 [CrossRef]
    [Google Scholar]
  10. Brock T. D., Brock K. M., Belly R. T., Weiss R. L. 1972; Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Microbiol 84:54–68
    [Google Scholar]
  11. Cascales E., Christie P. J. 2003; The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1:137–149 [CrossRef]
    [Google Scholar]
  12. Christie P. J. 2001; Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol Microbiol 40:294–305 [CrossRef]
    [Google Scholar]
  13. Christie P. J., Ward J. E. Jr, Gordon M. P., Nester E. W. 1989; A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. Proc Natl Acad Sci U S A 86:9677–9681 [CrossRef]
    [Google Scholar]
  14. Cohen-Krausz S., Trachtenberg S. 2002; The structure of the archeabacterial flagellar filament of the extreme halophile Halobacterium salinarum R1M1 and its relation to eubacterial flagellar filaments and type IV pili. J Mol Biol 321:383–395 [CrossRef]
    [Google Scholar]
  15. Craig L., Taylor R. K., Pique M. E. 9 other authors 2003; Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 11:1139–1150 [CrossRef]
    [Google Scholar]
  16. Elferink M. G. L., Albers S.-V., Konings W. N., Driessen A. J. M. 2001; Sugar transport in Sulfolobus solfataricus is mediated by two families of binding protein-dependent ABC transporters. Mol Microbiol 39:1494–1503 [CrossRef]
    [Google Scholar]
  17. Faguy D. M., Jarrell K. F., Kuzio J., Kalmokoff M. L. 1994; Molecular analysis of archael flagellins: similarity to the type IV pilin-transport superfamily widespread in bacteria. Can J Microbiol 40:67–71 [CrossRef]
    [Google Scholar]
  18. Herdendorf T. J., McCaslin D. R., Forest K. T. 2002; Aquifex aeolicus PilT, homologue of a surface motility protein, is a thermostable oligomeric NTPase. J Bacteriol 184:6465–6471 [CrossRef]
    [Google Scholar]
  19. Hobbs M., Mattick J. S. 1993; Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol 10:233–243 [CrossRef]
    [Google Scholar]
  20. Kachlany S. C., Planet P. J., Bhattacharjee M. K., Kollia E., Desalle R., Fine D. H., Figurski D. H. 2000; Nonspecific adherence by Actinobacillus actinomycetemcomitans requires genes widespread in bacteria and archaea. J Bacteriol 182:6169–6176 [CrossRef]
    [Google Scholar]
  21. Koenig H. 1988; Archaeobacterial cell envelopes. Can J Microbiol 34:395–406 [CrossRef]
    [Google Scholar]
  22. Krause S., Barcena M., Pansegrau W., Lurz R., Carazo J. M., Lanka E. 2000; Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by the cag pathogenicity island of Helicobacter pylori share similar hexameric ring structures. Proc Natl Acad Sci U S A 97:3067–3072 [CrossRef]
    [Google Scholar]
  23. Lanzetta P. A., Alvarez L. J., Reinach P. S., Candia O. A. 1979; An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100:95–97 [CrossRef]
    [Google Scholar]
  24. Lower B. H., Kennelly P. J. 2003; Open reading frame sso2387 from the archaeon Sulfolobus solfataricus encodes a polypeptide with protein-serine kinase activity. J Bacteriol 185:3436–3445 [CrossRef]
    [Google Scholar]
  25. Mattick J. S. 2002; Type IV pili and twitching motility. Annu Rev Microbiol 56:289–314 [CrossRef]
    [Google Scholar]
  26. Mattick J. S., Whitchurch C. B., Alm R. A. 1996; The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa – a review. Gene 179:147–155 [CrossRef]
    [Google Scholar]
  27. Merz A. J., So M., Sheetz M. P. 2000; Pilus retraction powers bacterial twitching motility. Nature 407:98–102 [CrossRef]
    [Google Scholar]
  28. Miroux B., Walker J. E. 1996; Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260:289–298 [CrossRef]
    [Google Scholar]
  29. Nunn D. N., Lory S. 1992; Components of the protein-excretion apparatus of Pseudomonas aeruginosa are processed by the type IV prepilin peptidase. Proc Natl Acad Sci U S A 89:47–51 [CrossRef]
    [Google Scholar]
  30. Patenge N., Berendes A., Engelhardt H., Schuster S. C., Oesterhelt D. 2001; The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum. Mol Microbiol 41:653–663 [CrossRef]
    [Google Scholar]
  31. Peabody C. R., Chung Y. J., Yen M. R., Vidal-Ingigliardi D., Pugsley A. P., Saier M. H. Jr 2003; Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051–3072 [CrossRef]
    [Google Scholar]
  32. Planet P. J., Kachlany S. C., Desalle R., Figurski D. H. 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 U S A 98:2503–2508 [CrossRef]
    [Google Scholar]
  33. Possot O. M., Pugsley A. P. 1994; Molecular characterization of PulE, a protein required for pullulanase secretion. Mol Microbiol 12:287–299 [CrossRef]
    [Google Scholar]
  34. Possot O. M., Pugsley A. P. 1997; The conserved tetracysteine motif in the general secretory pathway component PulE is required for efficient pullulanase secretion. Gene 192:45–50 [CrossRef]
    [Google Scholar]
  35. Prüschenk R., Baumeister W., Zillig W. 1987; Surface structure variants in different species of Sulfolobus. FEMS Microbiol Lett 43:327–330 [CrossRef]
    [Google Scholar]
  36. Pugsley A. P. 1993a; The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57:50–108
    [Google Scholar]
  37. Pugsley A. P. 1993b; Processing and methylation of PuIG, a pilin-like component of the general secretory pathway of Klebsiella oxytoca. Mol Microbiol 9:295–308 [CrossRef]
    [Google Scholar]
  38. Rivas S., Bolland S., Cabezon E., Goni F. M., de la Cruz C. F. 1997; TrwD, a protein encoded by the IncW plasmid R388, displays an ATP hydrolase activity essential for bacterial conjugation. J Biol Chem 272:25583–25590 [CrossRef]
    [Google Scholar]
  39. Robien M. A., Krumm B. E., Sandkvst M., Hol W. G. J. 2003; Crystal structure of the extracellular protein secretion NTPase EpsE of Vibrio cholerae . J Mol Biol 333:657–674 [CrossRef]
    [Google Scholar]
  40. Sagulenko E., Sagulenko V., Chen J., Christie P. J. 2001; Role of Agrobacterium VirB11 ATPase in T-pilus assembly and substrate selection. J Bacteriol 183:5813–5825 [CrossRef]
    [Google Scholar]
  41. Samatey F. A., Imada K., Nagashima S., Vonderviszt F., Kumasaka T., Yamamoto M., Namba K. 2001; Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331–337 [CrossRef]
    [Google Scholar]
  42. Sandkvist M. 2001; Biology of type II secretion. Mol Microbiol 40:271–283 [CrossRef]
    [Google Scholar]
  43. Sandkvist M., Bagdasarian M., Howard S. P., DiRita V. J. 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
    [Google Scholar]
  44. Savvides S. N., Yeo H. J., Beck M. R. & 7 other authors; 2003; VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J 22:1969–1980 [CrossRef]
    [Google Scholar]
  45. Sexton J. A., Pinkner J. S., Roth R., Heuser J. E., Hultgren S. J., Vogel J. P. 2004; The Legionella pneumophila PilT homologue DotB exhibits ATPase activity that is critical for intracellular growth. J Bacteriol 186:1658–1666 [CrossRef]
    [Google Scholar]
  46. Shevchik V. E., Robert-Baudouy J., Condemine G. 1997; Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins. EMBO J 16:3007–3016 [CrossRef]
    [Google Scholar]
  47. Tatusov R. L., Galperin M. Y., Natale D. A., Koonin E. V. 2000; The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36 [CrossRef]
    [Google Scholar]
  48. Thanassi D. G. 2002; Ushers and secretins: channels for the secretion of folded proteins across the bacterial outer membrane. J Mol Microbiol Biotechnol 4:11–20
    [Google Scholar]
  49. Thomas N. A., Mueller S., Klein A., Jarrell K. F. 2002; Mutants in flaI and flaJ of the archaeon Methanococcus voltae are deficient in flagellum assembly. Mol Microbiol 46:879–887 [CrossRef]
    [Google Scholar]
  50. Worthington P., Hoang V., Perez-Pomares F., Blum P. 2003; Targeted disruption of the alpha-amylase gene in the hyperthermophilic archaeon Sulfolobus solfataricus . J Bacteriol 185:482–488 [CrossRef]
    [Google Scholar]
  51. Yeo H., Savvides S. N., Herr A. B., Lanka E., Waksman G. 2000; Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion. Syst Mol Cell 6:1461–1472 [CrossRef]
    [Google Scholar]
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