The Journal of Membrane Biology

, Volume 214, Issue 1–2, pp 75–90 | Cite as

Protein Secretion and Membrane Insertion Systems in Gram-Negative Bacteria

Article

Abstract

In contrast to other organisms, gram-negative bacteria have evolved numerous systems for protein export. Eight types are known that mediate export across or insertion into the cytoplasmic membrane, while eight specifically mediate export across or insertion into the outer membrane. Three of the former secretory pathway (SP) systems, type I SP (ISP, ABC), IIISP (Fla/Path) and IVSP (Conj/Vir), can export proteins across both membranes in a single energy-coupled step. A fourth generalized mechanism for exporting proteins across the two-membrane envelope in two distinct steps (which we here refer to as type II secretory pathways [IISP]) utilizes either the general secretory pathway (GSP or Sec) or the twin-arginine targeting translocase for translocation across the inner membrane, and either the main terminal branch or one of several protein-specific export systems for translocation across the outer membrane. We here survey the various well-characterized protein translocation systems found in living organisms and then focus on the systems present in gram-negative bacteria. Comparisons between these systems suggest specific biogenic, mechanistic and evolutionary similarities as well as major differences.

Keywords

Protein Secretion Membrane insertion Transport Gram-negative bacteria 

References

  1. Adams J.M., Cory S. 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281:1322–1326PubMedGoogle Scholar
  2. Axelsson L., Holck A. 1995. The genes involved in production of and immunity to sakacin A, a bacteriocin from Lactobacillus sake Lb706. J. Bacteriol. 177:2125–2137PubMedGoogle Scholar
  3. Benach J., Chou Y.T., Fak J.J., Itkin A., Nicolae D.D., Smith P.C., Wittrock G., Floyd D.L., Golsaz C.M., Gierasch L.M., Hunt J.F. 2003. Phospholipid-induced monomerization and signal-peptide-induced oligomerization of SecA. J. Biol. Chem. 278:3628–3638PubMedGoogle Scholar
  4. Berks B.C., Palmer T., Sargent F. 2003. The Tat protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 47:187–254PubMedGoogle Scholar
  5. Berks B.C., Palmer T., Sargent F. 2005. Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr. Opin. Microbiol. 8:174–181PubMedGoogle Scholar
  6. Bogsch E.G., Sargent F., Stanley N.R., Berks B.C., Robinson C., Palmer T. 1998. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273:18003–18006PubMedGoogle Scholar
  7. Bohne J., Yim A., Binns A.N. 1998. The Ti plasmid increases the efficiency of Agrobacterium tumefaciens as a recipient in virB-mediated conjugal transfer of an IncQ plasmid. Proc. Natl. Acad. Sci. USA 95:7057–7062PubMedGoogle Scholar
  8. Bos M.P., Tefsen B., Geurtsen J., Tommassen J. 2004. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc. Natl. Acad. Sci. USA 101:9417–9422PubMedGoogle Scholar
  9. Burghout P., Beckers F., de Wit E., van Boxtel R., Cornelis G.R., Tommassen J., Koster M. 2004a. Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica. J. Bacteriol. 186:5366–5375Google Scholar
  10. Burghout P., van Boxtel R., Van Gelder P., Ringler P., Muller S.A., Tommassen J., Koster M. 2004b. Structure and electrophysiological properties of the YscC secretin from the type III secretion system of Yersinia enterocolitica. J. Bacteriol. 186:4645–4654Google Scholar
  11. Burrows L.L. 2005. Weapons of mass retraction. Mol. Microbiol. 57:878–888PubMedGoogle Scholar
  12. Busch W., Saier M.H. Jr. 2002. The transporter classification (TC) system, 2002. CRC Crit. Rev. Biochem. Mol. Biol. 37:287–337Google Scholar
  13. Cao T.B., Saier M.H. Jr. 2001. Conjugal type IV macromolecular transfer systems of gram-negative bacteria: Organismal distribution, structural constraints and evolutionary conclusions. Microbiology 147:3201–3214PubMedGoogle Scholar
  14. Cao T.B., Saier M.H. Jr. 2003. The general protein secretory pathway: Phylogenetic analyses leading to evolutionary conclusions. Biochim. Biophys. Acta 1609:115–125PubMedGoogle Scholar
  15. Chami M., Guilvout I., Gregorini M., Remigy H.W., Muller S.A., Valerio M., Engel A., Pugsley A.P., Bayan N. 2005. Structural insights into the secretin PulD and its trypsin-resistant core. J. Biol. Chem. 280:37732–37741PubMedGoogle Scholar
  16. Chang G., Roth C.B. 2001. Structure of MsbA from E. coli: A homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science 293:1793–1800PubMedGoogle Scholar
  17. Chen I., Christie P.J., Dubnau D. 2005. The ins and outs of DNA transfer in bacteria. Science 310:1456–1460PubMedGoogle Scholar
  18. Christie P.J. 2001. Type IV secretion: Intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294–305PubMedGoogle Scholar
  19. Christie P.J., Cascales E. 2005. Structural and dynamic properties of bacterial type IV secretion systems. Mol. Membr. Biol. 22:51–61PubMedGoogle Scholar
  20. Collins R.F., Davidsen L., Derrick J.P., Ford R.C., Tonjum T. 2001. Analysis of the PilQ secretion from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J. Bacteriol. 183:3825–3832PubMedGoogle Scholar
  21. Coombes B.K., Finlay B.B. 2005. Insertion of the bacterial type III translocon: Not your average needle stick. Trends Microbiol. 13:92–95PubMedGoogle Scholar
  22. Cornelis G.R. 2002. The Yersinia Ysc-Yop “type III” weaponry. Nat. Rev. Mol. Cell. Biol. 3:742–752PubMedGoogle Scholar
  23. Cotter S.E., Surana N.K., St. Geme J.W. III. 2005. Trimeric autotransporters: A distinct subfamily of autotransporter proteins. Trends Microbiol. 13:199–205PubMedGoogle Scholar
  24. Crompton M., Barksby E., Johnson N., Capano M. 2002. Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie 84:143–152PubMedGoogle Scholar
  25. Dabney-Smith C., Mori H., Cline K. 2006. Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J. Biol. Chem. 281:5476–5483PubMedGoogle Scholar
  26. Dinh T., Paulsen I.T., Saier M.H. Jr. 1994. A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J. Bacteriol. 176:3825–3831PubMedGoogle Scholar
  27. Doerrler W.T., Raetz C.R. 2005. Loss of outer membrane proteins without inhibition of lipid export in an Escherichia coli YaeT mutant. J. Biol. Chem. 280:27679–27687PubMedGoogle Scholar
  28. Dubnau D. 1999. DNA uptake in bacteria. Annu. Rev. Microbiol. 53:217–244PubMedGoogle Scholar
  29. Economou A. 2002. Bacterial secretome: The assembly manual and operating instructions. Mol. Membr. Biol. 19:159–169PubMedGoogle Scholar
  30. Ertel F., Mirus O., Bredemeier R., Moslavac S., Becker T., Schleiff E. 2005. The evolutionarily related β-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J. Biol. Chem. 280:28281–28289PubMedGoogle Scholar
  31. Eswaran J., Koronakis E., Higgins M.K., Hughes C., Koronakis V. 2004. Three’s company: Component structures bring a closer view of tripartite drug efflux pumps. Curr. Opin. Struct. Biol. 14:741–747PubMedGoogle Scholar
  32. Federici L., Du D., Walas F., Matsumura H., Fernandez-Recio J., McKeegan K.S., Borges-Walmsley M.I., Luisi B.F., Walmsley A.R. 2005. The crystal structure of the outer membrane protein VceC from the bacterial pathogen Vibrio cholerae at 1.8 Å resolution. J. Biol. Chem. 280:15307–15314PubMedGoogle Scholar
  33. Filloux A. 2004. The underlying mechanisms of type II protein secretion. Biochim. Biophys. Acta 1694:163–179PubMedGoogle Scholar
  34. Francetic O., Pugsley A.P. 2005. Towards the identification of type II secretion signals in a nonacylated variant of pullulanase from Klebsiella oxytoca. J. Bacteriol. 187:7045–7055PubMedGoogle Scholar
  35. Froderberg L., Houben E., Samuelson J.C., Chen M., Park S.K., Phillips G.J., Dalbey R., Luirink J., De Gier J.W. 2003. Versatility of inner membrane protein biogenesis in Escherichia coli. Mol. Microbiol. 47:1015–1027PubMedGoogle Scholar
  36. Geller B.L. 1991. Energy requirements for protein translocation across the Escherichia coli inner membrane. Mol. Microbiol. 5:2093–2098PubMedGoogle Scholar
  37. Genevrois S., Steeghs L., Roholl P., Letesson J.J., van der Ley P. 2003. The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J. 22:1780–1789PubMedGoogle Scholar
  38. Gentle I., Gabriel K., Beech P., Waller R., Lithgow T. 2004. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J. Cell Biol. 164:19–24PubMedGoogle Scholar
  39. Gentle I.E., Burri L., Lithgow T. 2005. Molecular architecture and function of the Omp85 family of proteins. Mol. Microbiol. 58:1216–1225PubMedCrossRefGoogle Scholar
  40. Gerard F., Cline K. 2006. Efficient twin arginine translocation (Tat) pathway transport of a precursor protein covalently anchored to its initial cpTatC binding site. J. Biol. Chem. 281:6130–6135PubMedGoogle Scholar
  41. Gohlke S.F., De Leeuw E., Stanley N.R., Palmer T., Saibil H.R., Berks B.C. 2001. Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268:3361–3367PubMedGoogle Scholar
  42. Gralnick J.A., Vali H., Lies D.P., Newman D.K. 2006. Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc. Natl. Acad. Sci. USA 103:4669–4674PubMedGoogle Scholar
  43. Hamilton H.L., Dominguez N.M., Schwartz K.J., Hackett K.T., Dillard J.P. 2005. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55:1704–1721PubMedGoogle Scholar
  44. Hansen-Wester I., Hensel M. 2001. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3:549–559PubMedGoogle Scholar
  45. Harley K.T., Djordjevic G.M., Tseng T.-T., Saier M.H. Jr. 2000. Membrane-fusion protein homologues in gram-positive bacteria. Mol. Microbiol. 36:516–517PubMedGoogle Scholar
  46. Hicks M.G., Lee P.A., Georgiou G., Berks B.C., Palmer T. 2005. Positive selection for loss-of-function tat mutations identifies critical residues required for TatA activity. J. Bacteriol. 187:2920–2925PubMedGoogle Scholar
  47. Higgins C.F., Linton K.J. 2004. The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11:918–926PubMedGoogle Scholar
  48. Higgins M.K., Bokma E., Koronakis E., Hughes C., Koronakis V. 2004a. Structure of the periplasmic component of a bacterial drug efflux pump. Proc. Natl. Acad. Sci. USA 101:9994–9999Google Scholar
  49. Higgins M.K., Eswaran J., Edwards P., Schertler G.F., Hughes C., Koronakis V. 2004b. Structure of the ligand-blocked periplasmic entrance of the bacterial multidrug efflux protein TolC. J. Mol. Biol. 342:697–702Google Scholar
  50. Holland I.B., Schmitt L., Young J. 2005. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol. Membr. Biol. 22:29–39PubMedGoogle Scholar
  51. Hueck C.J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379–433PubMedGoogle Scholar
  52. Ito K. 1992. SecY and integral membrane components of the Escherichia coli protein translocation system. Mol. Microbiol. 6:2423–2428PubMedCrossRefGoogle Scholar
  53. Jacob-Dubuisson F., Buisine C., Willery E., Renauld-Mongenie G., Locht C. 1997. Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries. J. Bacteriol. 179:775–783PubMedGoogle Scholar
  54. Jacob-Dubuisson F., El-Hamel C., Saint N., Guedin S., Willery E., Molle G., Locht C. 1999. Channel formation by FhaC, the outer membrane protein involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J. Biol. Chem. 274:37731–37735PubMedGoogle Scholar
  55. Jacob-Dubuisson F., Locht C., Antoine R. 2001. Two-partner secretion in gram-negative bacteria: A thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 40:306–313PubMedGoogle Scholar
  56. Johnson T.L., Abendroth J., Hol W.G., Sandkvist M. 2006. Type II secretion: From structure to function. FEMS Microbiol. Lett. 255:175–186PubMedGoogle Scholar
  57. Jongbloed J.D.H., Martin U., Antelmann H., Hecker M., Tjalsma H., Venema G., Bron S., van Dijl J.M., Müller J. 2000. TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem. 275:41350–41357PubMedGoogle Scholar
  58. Karavolos M.H., Roe A.J., Wilson M., Henderson J., Lee J.J., Gally D.L., Khan C.M. 2005. Type III secretion of the Salmonella effector protein SopE is mediated via an N-terminal amino acid signal and not an mRNA sequence. J. Bacteriol. 187:1559–1567PubMedGoogle Scholar
  59. Karnholz A., Hoefler C., Odenbreit S., Fischer W., Hofreuter D., Haas R. 2006. Functional and topological characterization of novel components of the comB DNA transformation competence system in Helicobacter pylori. J. Bacteriol. 188:882–893PubMedGoogle Scholar
  60. Karpowich N.K., Huang H.H., Smith P.C., Hunt J.F. 2003. Crystal structures of the BtuF periplasmic-binding protein for vitamin B12 suggest a functionally important reduction in protein mobility upon ligand binding. J. Biol. Chem. 278:8429–8434PubMedGoogle Scholar
  61. Kim, S.H., Chao, Y. Saier, M.H., Jr. 2006. Protein-translocating trimeric autotransporters of gram-negative bacteria. J. Bacteriol. 188:5655–5667PubMedGoogle Scholar
  62. Kinch L.N., Saier M.H. Jr. Grishin N.V. 2002. Sec61β – a component of the archaeal protein secretory system. Trends Biochem. Sci. 27:170–171PubMedGoogle Scholar
  63. Könninger U.W., Hobbie S., Benz R., Braun V. 1999. The haemolysin-secreting ShlB protein of the outer membrane of Serratia marcescens: Determination of surface-exposed residues and formation of ion-permeable pores by ShlB mutants in artificial lipid bilayer membranes. Mol. Microbiol. 32:1212–1225PubMedGoogle Scholar
  64. Koronakis V. 2003. TolC – the bacterial exit duct for proteins and drugs. FEBS Lett. 555:66–71PubMedGoogle Scholar
  65. Koronakis V., Eswaran J., Hughes C. 2004. Structure and function of TolC: The bacterial exit duct for proteins and drugs. Annu. Rev. Biochem. 73:467–489PubMedGoogle Scholar
  66. Koronakis V., Sharff A., Koronakis E., Luisi B., Hughes C. 2000. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914–919PubMedGoogle Scholar
  67. Kozjak V., Wiedemann N., Milenkovic D., Lohaus C., Meyer H.E., Guiard B., Meisinger C., Pfanner N. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J. Biol. Chem. 278:48520–48523PubMedGoogle Scholar
  68. Kuan G., Dassa E., Saurin W., Hofnung M., Saier M.H. Jr. 1995. Phylogenic analyses of the ATP-binding constituents of bacterial extracytoplasmic receptor-dependent ABC-type nutrient uptake permeases. Res. Microbiol. 146:271–278PubMedGoogle Scholar
  69. Lee S.H., Galán J.E. 2004. Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol. Microbiol. 51:483–495PubMedGoogle Scholar
  70. Li J., Wolf S.G., Elbaum M., Tzfira T. 2005. Exploring cargo transport mechanics in the type IV secretion systems. Trends Microbiol. 13:295–298PubMedGoogle Scholar
  71. Lister R., Hulett J.M., Lithgow T., Whelan J. 2005. Protein import into mitochondria: Origins and functions today. Mol. Membr. Biol. 22:87–100PubMedGoogle Scholar
  72. Locher K.P., Lee A.T., Rees D.C. 2002. The E. coli BtuCD structure: A framework for ABC transporter architecture and mechanism. Science 296:1091–1098PubMedGoogle Scholar
  73. Loveless B.J., Saier M.H. Jr. 1997. A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol. Membr. Biol. 14:113–123PubMedGoogle Scholar
  74. Luirink J., Samuelsson T., de Gier J.-W. 2001. YidC/Oxa1p/Alb3: Evolutionarily conserved mediators of membrane protein assembly. FEBS Lett. 501:1–5PubMedGoogle Scholar
  75. Luirink J., von Heijne G., Houben E., de Gier J.W. 2005. Biogenesis of inner membrane proteins in Escherichia coli. Annu. Rev. Microbiol. 59:329–355PubMedGoogle Scholar
  76. Lybarger S.R., Sandkvist M. 2004. A hitchhiker’s guide to type IV secretion. Science 304:1122–1123PubMedGoogle Scholar
  77. Ma Q., Zhai Y., Schneider C.J., Ramseier T.M., Saier M.H. Jr. 2003. Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens. Biochim. Biophys. Acta 1611:223–233Google Scholar
  78. Mangels D., Mathers J., Bolhuis A., Robinson C. 2005. The core TatABC complex of the twin-arginine translocase in Escherichia coli: TatC drives assembly where TatA is essential for stability. J. Mol. Biol. 345:415–423PubMedGoogle Scholar
  79. Milenkovic D., Kozjak V., Wiedemann N., Lohaus C., Meyer H.E., Guiard B., Pfanner N., Meisinger C. 2004. Sam35 of the mitochondrial protein sorting and assembly machinery is a peripheral outer membrane protein essential for cell viability. J. Biol. Chem. 279:22781–22785PubMedGoogle Scholar
  80. Missiakas D., Betton J.M., Raina S. 1996. New components of protein folding in extracytoplasmic compartments of Escherichia coli, SurA, FkpA and Skp/OmpH. Mol. Microbiol. 21:871–886PubMedGoogle Scholar
  81. Mol O., Oudega B. 1996. Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol. Rev. 19:25–52PubMedGoogle Scholar
  82. Mota L.J., Cornelis G.R. 2005. The bacterial injection kit: Type III secretion systems. Ann. Med. 37:234–249PubMedGoogle Scholar
  83. Müller M. 2005. Twin-arginine-specific protein export in Escherichia coli. Res. Microbiol. 156:131–136PubMedGoogle Scholar
  84. Müller M., Klosgen R.B. 2005. The Tat pathway in bacteria and chloroplasts. Mol. Membr. Biol. 22:113–121PubMedGoogle Scholar
  85. Müller M., Koch H.-G., Beck K., Schäfer U. 2001. Protein traffic in bacteria: Multiple routes from the ribosome to and across the membrane. Prog. Nucleic Acid Res. Mol. Biol. 66:107–157PubMedCrossRefGoogle Scholar
  86. Newman C.L., Stathopoulos C. 2004. Autotransporter and two-partner secretion: Delivery of large-size virulence factors by gram-negative bacterial pathogens. Crit. Rev. Microbiol. 30:275–286PubMedGoogle Scholar
  87. Nguyen L., Paulsen I.T., Tchieu J., Hueck C.J., Saier M.H. Jr. 2000. Phylogenetic analyses of the constituents of type III protein secretion systems. J. Mol. Microbiol. Biotechnol. 2:125–144PubMedGoogle Scholar
  88. Nouwen N., Ranson N., Saibil H., Wolpensinger B., Engel A., Ghazi A., Pugsley A.P. 1999. Secretin PulD: Association with pilot PulS, structure, and ion-conducting channel formation. Proc. Natl. Acad. Sci. USA 96:8173–8177PubMedGoogle Scholar
  89. Nouwen N., van der Laan M., Driessen A.J. 2001. SecDFyajC is not required for the maintenance of the proton motive force. FEBS Lett. 508:103–106PubMedGoogle Scholar
  90. Oloo E.O., Tieleman D.P. 2004. Conformational transitions induced by the binding of MgATP to the vitamin B12 ATP-binding cassette (ABC) transporter BtuCD. J. Biol. Chem. 279:45013–45019PubMedGoogle Scholar
  91. Olsson J., Edqvist P.J., Bröms J.E., Forsberg A., Wolf-Watz H., Francis M.S. 2004. The YopD translocator of Yersinia pseudotuberculosis is a multifunctional protein comprised of discrete domains. J. Bacteriol. 186:4110–4123PubMedGoogle Scholar
  92. Palmer T., Sargent F., Berks B.C. 2005. Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol. 13:175–180PubMedGoogle Scholar
  93. Pantoja M., Chen L., Chen Y., Nester E.W. 2002. Agrobacterium type IV secretion is a two-step process in which export substrates associate with the virulence protein VirJ in the periplasm. Mol. Microbiol. 45:1325–1335PubMedGoogle Scholar
  94. Paulsen I.T., Beness A.M., Saier M.H. Jr. 1997a. Computer-based analyses of the protein constituents of transport systems catalysing export of complex carbohydrates in bacteria. Microbiology 143:2685–2699CrossRefGoogle Scholar
  95. Paulsen I.T., Park J.H., Choi P.S., Saier M.H. Jr. 1997b. A family of gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from gram-negative bacteria. FEMS Microbiol. Lett. 156:1–8CrossRefGoogle Scholar
  96. 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 149:3051–3072PubMedGoogle Scholar
  97. Pivetti C.D., Yen M.-R., Miller S., Busch W., Tseng Y.-H., Booth I.R., Saier M.H. Jr. 2003. Two families of mechanosensitive channel proteins. Microbiol. Mol. Biol. Rev. 67:66–85PubMedGoogle Scholar
  98. Plano G.V., Day J.B., Ferracci F. 2001. Type III export: New uses for old pathway. Mol. Microbiol. 40:284–293PubMedGoogle Scholar
  99. Pohlschroder M., Hartmann E., Hand N.J., Dilks K., Haddad A. 2005. Diversity and evolution of protein translocation. Annu. Rev. Microbiol. 59:91–111PubMedGoogle Scholar
  100. Quadri L.E., Kleerebezem M., Kuipers O.P., de Vos W.M., Roy K.L., Vederas J.C., Stiles M.E. 1997. Characterization of a locus from Carnobacterium piscicola LV17B involved in bacteriocin production and immunity: Evidence for global inducer-mediated transcriptional regulation. J. Bacteriol. 179:6163–6171PubMedGoogle Scholar
  101. Ramamurthi K.S., Schneewind O. 2003a. Substrate recognition by the Yersinia type III protein secretion machinery. Mol. Microbiol. 50:1095–1102Google Scholar
  102. Ramamurthi K.S., Schneewind O. 2003b. Yersinia yopQ mRNA encodes a bipartite type III secretion signal in the first 15 codons. Mol. Microbiol. 50:1189–1198Google Scholar
  103. Ramanculov E., Young R. 2001. Genetic analysis of the T4 holin: Timing and topology. Gene 265:25–36PubMedGoogle Scholar
  104. Rapoport T.A., Goder V., Heinrich S.U., Matlack K.E. 2004. Membrane-protein integration and the role of the translocation channel. Trends Cell. Biol. 14:568–575PubMedGoogle Scholar
  105. Rapoport T.A., Jungnickel B., Kutay U. 1996. Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem. 65:271–303PubMedGoogle Scholar
  106. Reyes C.L., Chang G. 2005. Lipopolysaccharide stabilizes the crystal packing of the ABC transporter MsbA. Acta Crystallogr. F Struct. Biol. Cryst. Commun. 61:655–658Google Scholar
  107. Robinson C., Woolhead C., Edwards W. 2000. Transport of proteins into and across the thylakoid membrane. J. Exp. Bot. 51(Special issue):369–374PubMedGoogle Scholar
  108. Roggenkamp, A., Ackermann, N., Jacobi, C.A., Truelzsch, K., Hoffmann, H., Heesemann, J. 2003. Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YasA. J. Bactorial. 185:3735–3744Google Scholar
  109. Ryndak M.B., Chung H., London E., Bliska J.B. 2005. Role of predicted transmembrane domains for type III translocation, pore formation, and signaling by the Yersinia pseudotuberculosis YopB protein. Infect. Immun. 73:2433–2443PubMedGoogle Scholar
  110. Saier M.H. Jr. 1998. Molecular phylogeny as a basis for the classification of transport proteins from bacteria, archaea and eukarya. In: Poole R.K., editor. Advances in Microbial Physiology, Academic Press, San Diego pp 81–136Google Scholar
  111. Saier M.H. Jr. 1999. A functional-phylogenetic system for the classification of transport proteins. J. Cell. Biochem. Suppl. 32/33:84–94Google Scholar
  112. Saier M.H. Jr. 2000a. A functional/phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64:354–411Google Scholar
  113. Saier M.H. Jr. 2000b. Families of proteins forming transmembrane channels. J. Membr. Biol. 175:165–180Google Scholar
  114. Saier M.H. Jr. 2004. Evolution of bacterial type III protein secretion systems. Trends Microbiol. 12:113–115PubMedGoogle Scholar
  115. Saier M.H. Jr., Tran C.V., Barabote R.D. 2006. TCDB: The transporter classification database for membrane transport protein analyses and information. Nucleic Acids Res. 34:D181–D186PubMedGoogle Scholar
  116. Saier M.H., Jr., Tseng T.-T. 1999. Evolutionary origins of transmembrane transport systems. In: Broome-Smith J.K., Baumberg S., Stirling C.J., Ward F.B. editors. Transport of Molecules Across Microbial Membranes. Symposium 58, Society for General Microbiology, Cambridge University Press, Cambridge pp 252–274Google Scholar
  117. Sambasivarao D., Dawson H.A., Zhang G., Shaw G., Hu J., Weiner J.H. 2001. Investigation of Escherichia coli dimethyl sulfoxide reductase assembly and processing in strains defective for the sec-independent protein translocation system membrane targeting and translocation. J. Biol. Chem. 276:20167–20174PubMedGoogle Scholar
  118. Sambasivarao D., Turner R.J., Bilous P.T., Rothery R.A., Shaw G., Weiner J.H. 2002. Differential effects of a molybdopterin synthase sulfurylase (moeB) mutation on Escherichia coli molybdoenzyme maturation. Biochem. Cell. Biol. 80:435–443PubMedGoogle Scholar
  119. Sambasivarao D., Turner R.J., Simala-Grant J.L., Shaw G., Hu J., Weiner J.H. 2000. Multiple roles for the twin arginine leader sequence of dimethyl sulfoxide reductase of Escherichia coli. J. Biol. Chem. 275:22526–22531PubMedGoogle Scholar
  120. Sandkvist M, 2001. Biology of type II secretion. Mol. Microbiol. 40:271–283PubMedGoogle Scholar
  121. Sargent F., Berks B.C., Palmer T. 2006. Pathfinders and trailblazers: a prokaryotic targeting system for transport of folded proteins. FEMS Microbiol. Lett. 254:198–207PubMedCrossRefGoogle Scholar
  122. Sargent F., Gohlke U., De Leeuw E., Stanley N.R., Palmer T., Saibil H.R., Berks B.C. 2001. Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268:3361–3667PubMedGoogle Scholar
  123. Sargent F., Stanley N.R., Berks B.C., Palmer T. 1999. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem. 274:36073–36082PubMedGoogle Scholar
  124. Sauer F.G., Knight S.D., Waksman G.J., Hultgren S.J. 2000. PapD-like chaperones and pilus biogenesis. Semin. Cell Dev. Biol. 11:27–34PubMedGoogle Scholar
  125. Scheuring J., Braun N., Nothdurft L., Stumpf M., Veenendaal A.K., Kol S., van der Does C., Driessen A.J., Weinkauf S. 2005. The oligomeric distribution of SecYEG is altered by SecA and translocation ligands. J. Mol. Biol. 354:258–271PubMedGoogle Scholar
  126. Schleiff E., Soll J., Küchler M., Kühlbrandt W., Harrer R. 2003. Characterization of the translocon of the outer envelope of chloroplasts. J. Cell Biol. 160:541–551PubMedGoogle Scholar
  127. Schmidt S.A., Bieber D., Ramer S.W., Hwang J., Wu C.Y., Schoolnik G. 2001. Structure-function analysis of BfpB, a secretin-like protein encoded by the bundle-forming-pilus operon of enteropathogenic Escherichia coli. J. Bacteriol. 183:4848–4859PubMedGoogle Scholar
  128. Schmitt L., Benabdelhak H., Blight M.A., Holland I.B., Stubbs M.T. 2003. Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: Identification of a variable region within ABC helical domains. J. Mol. Biol. 330:333–342PubMedGoogle Scholar
  129. Scotti P.A., Valent Q.A., Manting E.H., Urbanus M.L., Driessen A.J., Oudega B., Luirink J. 1999. SecA is not required for signal recognition particle-mediated targeting and initial membrane insertion of a nascent inner membrane protein. J. Biol. Chem. 274:29883–29888PubMedGoogle Scholar
  130. Sijbrandi R., Urbanus M.L., ten Hagen-Jongman C.M., Bernstein H.D., Oudega B., Otto B.R., Luirink J. 2003. Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J. Biol. Chem. 278:4654–4659PubMedGoogle Scholar
  131. Stanley N.R., Sargent F., Buchanan G., Shi J., Stewart V., Palmer T., Berks B.C. 2002. Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol. Microbiol. 43:1005–1021PubMedGoogle Scholar
  132. Steiner J.M., Yusa F., Pompe J.A., Loffelhardt W. 2005. Homologous protein import machineries in chloroplasts and cyanelles. Plant J. 44:646–652PubMedGoogle Scholar
  133. Takamatsu H., Bunai K., Horinaka T., Oguro A., Nakamura K., Watabe K., Yamane K. 1997. Identification of a region required for binding to presecretory protein in Bacillus subtilis Ffh, a homologue of the 54-kDa subunit of mammalian signal recognition particle. Eur. J. Biochem. 248:575–582PubMedGoogle Scholar
  134. Tam R., Saier M.H. Jr. 1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57:320–346PubMedGoogle Scholar
  135. Thanassi D.G. 2002. Ushers and secretins: Channels for the secretion of folded proteins across the bacterial outer membrane. J. Mol. Microbiol. Biotechnol. 4:11–20PubMedGoogle Scholar
  136. Thanassi D.G., Hultgren S.J. 2000. Assembly of complex organelles: Pilus biogenesis in gram-negative bacteria as a model system. Methods 20:111–126PubMedGoogle Scholar
  137. Thanassi D.G., Stathopoulos C., Karkal A., Li H. 2005. Protein secretion in the absence of ATP: The autotransporter, two-partner secretion and chaperone/usher pathways of gram-negative bacteria. Mol. Membr. Biol. 22:63–72PubMedGoogle Scholar
  138. Theg, S.M., Cline, K., Finazzi, G., Wollman, F.A. 2005. The energetics of the chloroplast Tat protein transport pathway revisited. Trends Plant Sci. 10:153–154Google Scholar
  139. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. 1997. The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876–4882PubMedGoogle Scholar
  140. Touze T., Eswaran J., Bokma E., Koronakis E., Hughes C., Koronakis V. 2004. Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol. Microbiol. 53:697–706PubMedGoogle Scholar
  141. Tziatzios C., Schubert D., Lotz M., Gundogan D., Betz H., Schagger H., Haase W., Duong F., Collinson I. 2004. The bacterial protein-translocation complex: SecYEG dimers associate with one or two SecA molecules. J. Mol. Biol. 340:513–524PubMedGoogle Scholar
  142. van den Berg B., Clemons W.M. Jr., Collinson I., Modis Y., Hartmann E., Harrison S.C., Rapoport T.A. 2004. X-ray structure of a protein-conducting channel. Nature 427:36–44PubMedGoogle Scholar
  143. van der Laan M., Nouwen N.P., Driessen A.J. 2005. YidC – an evolutionary conserved device for the assembly of energy-transducing membrane protein complexes. Curr. Opin. Microbiol. 8:182–187PubMedGoogle Scholar
  144. van Dijl J.M., Braun P.G., Robinson C., Quax W.J., Antelmann H., Hecker M., Muller J., Tjalsma H., Bron S., Jongbloed J.D. 2002. Functional genomic analysis of the Bacillus subtilis Tat pathway for protein secretion. J. Biotechnol. 98:243–254PubMedGoogle Scholar
  145. Van Rosmalen M., Saier M.H. Jr. 1993. Structural and evolutionary relationships between two families of bacterial extracytoplasmic chaperone proteins which function cooperatively in fimbrial assembly. Res. Microbiol. 144:507–527PubMedGoogle Scholar
  146. Veiga E., Sugawara E., Nikaido H., de Lorenzo V., Fernández L.A. 2002. Export of autotransported proteins proceeds through an oligomeric ring shape by C-terminal domains. EMBO J. 21:2122–2131PubMedGoogle Scholar
  147. Venema K., Dost M.H., Beun P.A., Haandrikman A.J., Venema G., Kok J. 1996. The genes for secretion and maturation of lactococcins are located on the chromosome of Lactococcus lactis IL1403. Appl. Environ. Microbiol. 62:1689–1692PubMedGoogle Scholar
  148. Vignon G., Kohler R., Larquet E., Giroux S., Prevost M.C., Roux P., Pugsley A.P. 2003. Type IV-like pili formed by the type II secreton: Specificity, composition, bundling, polar localization, and surface presentation of peptides. J. Bacteriol. 185:3416–3428PubMedGoogle Scholar
  149. Voulhoux R., Bos M.P., Geurtsen J., Mols M., Tommassen J. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262–265PubMedGoogle Scholar
  150. Wang I.-N., Smith D.L., Young R. 2000. Holins: The protein clocks of bacteriophage infections. Annu. Rev. Microbiol. 54:799–825PubMedGoogle Scholar
  151. Wickner W., Schekman R. 2005. Protein translocation across biological membranes. Science 310:1452–1456PubMedGoogle Scholar
  152. Wiedemann N., Kozjak V., Chacinska A., Schönfisch B., Rospert S., Ryan M.T., Pfanner N., Meisinger C. 2003. Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424:565–571PubMedGoogle Scholar
  153. Winans S.C., Burns D.L., Christie P.J. 1996. Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 4:64–68PubMedGoogle Scholar
  154. Wu T., Malinverni J., Ruiz N., Kim S., Silhavy T.J., Kahne D. 2005. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235–245PubMedGoogle Scholar
  155. Yamane K., Bunai K., Kakeshita H. 2004. Protein traffic for secretion and related machinery of Bacillus subtilis. Biosci. Biotechnol. Biochem. 68:2007–2023PubMedGoogle Scholar
  156. Yen M.-R., Harley K.T., Tseng Y.-H., Saier M.H. Jr. 2001. Phylogenetic and structural analyses of the Oxa1 family of protein translocases. FEMS Microbiol Lett. 204:223–231PubMedGoogle Scholar
  157. Yen M.-R., Peabody C.R., Partovi S.M., Zhai Y., Tseng Y.-H., Saier M.H. Jr. 2002a. Protein-translocating outer membrane porins of gram-negative bacteria. Biochim. Biophys. Acta 1562:6–31Google Scholar
  158. Yen M.-R., Tseng Y.-H., Nguyen E.H., Wu L.F., Saier M.H. Jr. 2002b. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol. 177:441–450Google Scholar
  159. Yi L., Dalbey R.E. 2005. Oxa1/Alb3/YidC system for insertion of membrane proteins in mitochondria, chloroplasts and bacteria. Mol. Membr. Biol. 22:101–111PubMedGoogle Scholar
  160. Yip C.K., Kimbrough T.G., Felise H.B., Vuckovic M., Thomas N.A., Pfuetzner R.A., Frey E.A., Finlay B.B., Miller S.I., Strynadka N.C. 2005. Structural characterization of the molecular platform for type III secretion system assembly. Nature 435:702–707PubMedGoogle Scholar
  161. Young G.M., Schmiel D.H., Miller V.L. 1999. A new pathway for the secretion of virulence factors by bacteria, the flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci. USA 96:6456–6461PubMedGoogle Scholar
  162. Young R. 2002. Bacteriophage holins: Deadly diversity. J. Mol. Microbiol. Biotechnol. 4:21–36PubMedGoogle Scholar
  163. Young R., Bläsi U. 1995. Holins: Form and function in bacteriophage lysis. FEMS Microbiol. Rev. 17:191–205PubMedGoogle Scholar
  164. Zhai Y., Tchieu J., Saier M.H. Jr. 2002. A web-based Tree View (TV) program for the visualization of phylogenetic trees. J. Mol. Microbiol. Biotechnol. 4:69–70PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Division of Biological SciencesUniversity of California at San DiegoLa Jolla

Personalised recommendations