Table of Contents Author Guidelines Submit a Manuscript
Archaea
Volume 2010, Article ID 608243, 13 pages
http://dx.doi.org/10.1155/2010/608243
Review Article

Shaping the Archaeal Cell Envelope

1Centre for Integrative Biology, Microbial Genomics, Via delle Regole 101, 38123 Mattarello, Italy
2Department of Molecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, The Zernike Institute for Advanced Materials, University of Groningen, Kerklaan 30, 9751 NN Haren, The Netherlands
3Molecular Biology of Archaea, Max Planck Institute for terrestrial Microbiology, Karl-von-Frisch-Straße 10, 35043 Marburg, Germany

Received 14 April 2010; Accepted 29 May 2010

Academic Editor: Jerry Eichler

Copyright © 2010 Albert F. Ellen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Koenig, “Archaeobacterial cell envelopes,” Canadian Journal of Microbiology, vol. 34, pp. 395–406, 1988. View at Google Scholar
  2. R. Rachel, I. Wyschkony, S. Riehl, and H. Huber, “The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon,” Archaea, vol. 1, no. 1, pp. 9–18, 2002. View at Google Scholar · View at Scopus
  3. M. Kates, “Structural analysis of phospholipids and glycolipids in extremely halophilic archaebacteria,” Journal of Microbiological Methods, vol. 25, no. 2, pp. 113–128, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. M. De Rosa, A. Gambacorta, B. Nicolaus, B. Chappe, and P. Albrecht, “Isoprenoid ethers; backbone of complex lipids of the archaebacterium Sulfolobus solfataricus,” Biochimica et Biophysica Acta (BBA), vol. 753, no. 2, pp. 249–256, 1983. View at Google Scholar · View at Scopus
  5. M. De Rosa, A. Trincone, B. Nicolaus, A. Gambacorta, and G. di Prisco, “Archaebacteria: lipids, membrane structures, and adaptations to environmental stresses,” in Life under Extreme Conditions, pp. 61–87, Springer, Berlin, Germany, 1991. View at Google Scholar
  6. J. L. C. M. Van de Vossenberg, T. Ubbink-Kok, M. G. L. Elferink, A. J. M. Driessen, and W. N. Konings, “Ion permeability of the cytoplasmic membrane limits the maximum growth temperature of bacteria and archaea,” Molecular Microbiology, vol. 18, no. 5, pp. 925–932, 1995. View at Google Scholar · View at Scopus
  7. O. Kandler and H. Koenig, “Chemical composition of the peptidoglycan-free cell walls of methanogenic bacteria,” Archives of Microbiology, vol. 118, no. 2, pp. 141–152, 1978. View at Google Scholar · View at Scopus
  8. A. J. M. Driessen and N. Nouwen, “Protein translocation across the bacterial cytoplasmic membrane,” Annual Review of Biochemistry, vol. 77, pp. 643–667, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. A. M. Flower, L. L. Hines, and P. L. Pfennig, “SecG is an auxiliary component of the protein export apparatus of Escherichia coli,” Molecular and General Genetics, vol. 263, no. 1, pp. 131–136, 2000. View at Google Scholar · View at Scopus
  10. L. N. Kinch, M. H. Saier Jr., and N. V. Grishin, “Sec61β—a component of the archaeal protein secretory system,” Trends in Biochemical Sciences, vol. 27, no. 4, pp. 170–171, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. S.-V. Albers, Z. Szabó, and A. J. M. Driessen, “Protein secretion in the Archaea: multiple paths towards a unique cell surface,” Nature Reviews Microbiology, vol. 4, no. 7, pp. 537–547, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Van den Berg, W. M. Clemons Jr., I. Collinson et al., “X-ray structure of a protein-conducting channel,” Nature, vol. 427, no. 6969, pp. 36–44, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Ring and J. Eichler, “Extreme secretion: protein translocation across the archael plasma membrane,” Journal of Bioenergetics and Biomembranes, vol. 36, no. 1, pp. 35–45, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. V. Irihimovitch and J. Eichler, “Post-translational secretion of fusion proteins in the halophilic archaea Haloferax volcanii,” The Journal of Biological Chemistry, vol. 278, no. 15, pp. 12881–12887, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. N. J. Hand, R. Klein, A. Laskewitz, and M. Pohlschröder, “Archaeal and bacterial SecD and SecF homologs exhibit striking structural and functional conservation,” Journal of Bacteriology, vol. 188, no. 4, pp. 1251–1259, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. D. J. F. du Plessis, G. Berrelkamp, N. Nouwen, and A. J. M. Driessen, “The lateral gate of SecYEG opens during protein translocation,” The Journal of Biological Chemistry, vol. 284, no. 23, pp. 15805–15814, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Robinson and A. Bolhuis, “Tat-dependent protein targeting in prokaryotes and chloroplasts,” Biochimica et Biophysica Acta, vol. 1694, no. 1–3, pp. 135–147, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Dilks, R. W. Rose, E. Hartmann, and M. Pohlschröder, “Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey,” Journal of Bacteriology, vol. 185, no. 4, pp. 1478–1483, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Dilks, M. I. Giménez, and M. Pohlschröder, “Genetic and biochemical analysis of the twin-arginine translocation pathway in halophilic archaea,” Journal of Bacteriology, vol. 187, no. 23, pp. 8104–8113, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. D. C. Kwan, J. R. Thomas, and A. Bolhuis, “Bioenergetic requirements of a Tat-dependent substrate in the halophilic archaeon Haloarcula hispanica,” FEBS Journal, vol. 275, no. 24, pp. 6159–6167, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. D. A. Widdick, K. Dilks, G. Chandra et al., “The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 47, pp. 17927–17932, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. G. von Heijne, “The signal peptide,” Journal of Membrane Biology, vol. 115, no. 3, pp. 195–201, 1990. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Tullman-Ercek, M. P. DeLisa, Y. Kawarasaki et al., “Export pathway selectivity of Escherichia coli twin arginine translocation signal peptides,” The Journal of Biological Chemistry, vol. 282, no. 11, pp. 8309–8316, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. J. W. Izard and D. A. Kendall, “Signal peptides: exquisitely designed transport promoters,” Molecular Microbiology, vol. 13, no. 5, pp. 765–773, 1994. View at Google Scholar · View at Scopus
  25. M. P. DeLisa, D. Tullman, and G. Georgiou, “Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 10, pp. 6115–6120, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Richter, U. Lindenstrauss, C. Lücke, R. Bayliss, and T. Brüser, “Functional tat transport of unstructured, small, hydrophilic proteins,” The Journal of Biological Chemistry, vol. 282, no. 46, pp. 33257–33264, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. I. B. Holland, L. Schmitt, and J. Young, “Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway,” Molecular Membrane Biology, vol. 22, no. 1-2, pp. 29–39, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Cannio, A. D'Angelo, M. Rossi, and S. Bartolucci, “A superoxide dismutase from the archaeon Sulfolobus solfataricus is an extracellular enzyme and prevents the deactivation by superoxide of cell- bound proteins,” European Journal of Biochemistry, vol. 267, no. 1, pp. 235–243, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. A. F. Ellen, S.-V. Albers, and A. J. M. Driessen, “Comparative study of the extracellular proteome of Sulfolobus species reveals limited secretion,” Extremophiles, vol. 14, no. 1, pp. 87–98, 2010. View at Google Scholar
  30. G. Palmieri, R. Cannio, I. Fiume, M. Rossi, and G. Pocsfalvi, “Outside the unusual cell wall of the hyperthermophilic archaeon Aeropyrum pernix K1,” Molecular and Cellular Proteomics, vol. 8, no. 11, pp. 2570–2581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. P. K. Chong and P. C. Wright, “Identification and characterization of the Sulfolobus solfataricus P2 proteome,” Journal of Proteome Research, vol. 4, no. 5, pp. 1789–1798, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Filloux, “The underlying mechanisms of type II protein secretion,” Biochimica et Biophysica Acta, vol. 1694, no. 1–3, pp. 163–179, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Voulhoux, G. Ball, B. Ize et al., “Involvement of the twin-arginine translocation system in protein secretion via the type II pathway,” EMBO Journal, vol. 20, no. 23, pp. 6735–6741, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Chen, P. J. Christie, and D. Dubnau, “The ins and outs of DNA transfer in bacteria,” Science, vol. 310, no. 5753, pp. 1456–1460, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Fronzes, E. Schäfer, L. Wang, H. R. Saibil, E. V. Orlova, and G. Waksman, “Structure of a type IV secretion system core complex,” Science, vol. 323, no. 5911, pp. 266–268, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. Q. She, H. Phan, R. A. Garrett, S.-V. Albers, K. M. Stedman, and W. Zillig, “Genetic profile of pNOB8 from Sulfolobus: the first conjugative plasmid from an archaeon,” Extremophiles, vol. 2, no. 4, pp. 417–425, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Erauso, K. M. Stedman, H. J. G. van den Werken, W. Zillig, and J. van der Oost, “Two novel conjugative plasmids from a single strain of Sulfolobus,” Microbiology, vol. 152, no. 7, pp. 1951–1968, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Prangishvili, S.-V. Albers, I. Holz et al., “Conjugation in archaea: frequent occurrence of conjugative plasmids in Sulfolobus,” Plasmid, vol. 40, no. 3, pp. 190–202, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. K. M. Stedman, Q. She, H. Phan et al., “pING family of conjugative plasmids from the extremely thermophilic archaeon Sulfolobus islandicus: insights into recombination and conjugation in Crenarchaeota,” Journal of Bacteriology, vol. 182, no. 24, pp. 7014–7020, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. I. Rosenshine, R. Tchelet, and M. Mevarech, “The mechanism of DNA transfer in the mating system of an archaebacterium,” Science, vol. 245, no. 4924, pp. 1387–1389, 1989. View at Google Scholar · View at Scopus
  41. L. Craig and J. Li, “Type IV pili: paradoxes in form and function,” Current Opinion in Structural Biology, vol. 18, no. 2, pp. 267–277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. M. S. Strom, D. N. Nunn, and S. Lory, “A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 6, pp. 2404–2408, 1993. View at Google Scholar · View at Scopus
  43. S. Y. M. Ng, B. Zolghadr, A. J. M. Driessen, S.-V. Albers, and K. F. Jarrell, “Cell surface structures of archaea,” Journal of Bacteriology, vol. 190, no. 18, pp. 6039–6047, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. P. J. Planet, S. C. Kachlany, R. DeSalle, and D. H. Figurski, “Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 5, pp. 2503–2508, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Yamagata and J. A. Tainer, “Hexameric structures of the archaeal secretion ATPase GspE and implications for a universal secretion mechanism,” EMBO Journal, vol. 26, no. 3, pp. 878–890, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. S.-V. Albers and A. J. M. Driessen, “Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus: a genomic survey,” Archives of Microbiology, vol. 177, no. 3, pp. 209–216, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. N. F. W. Saunders, C. Ng, M. Raftery, M. Guilhaus, A. Goodchild, and R. Cavicchioli, “Proteomic and computational analysis of secreted proteins with type I signal peptides from the antarctic archaeon Methanococcoides burtonii,” Journal of Proteome Research, vol. 5, no. 9, pp. 2457–2464, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Eichler and M. W. W. Adams, “Posttranslational protein modification in Archaea,” Microbiology and Molecular Biology Reviews, vol. 69, no. 3, pp. 393–425, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. M. I. Giménez, K. Dilks, and M. Pohlschröder, “Haloferax volcanii twin-arginine translocation substates include secreted soluble, C-terminally anchored and lipoproteins,” Molecular Microbiology, vol. 66, no. 6, pp. 1597–1606, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. S.-V. Albers, Z. Szabó, and A. J. M. Driessen, “Archaeal homolog of bacterial type IV prepilin signal peptidases with broad substrate specificity,” Journal of Bacteriology, vol. 185, no. 13, pp. 3918–3925, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. S. L. Bardy and K. F. Jarrell, “FlaK of the archaeon Methanococcus maripaludis possesses preflagellin peptidase activity,” FEMS Microbiology Letters, vol. 208, no. 1, pp. 53–59, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. Z. Szabó, A. O. Stahl, S.-V. Albers, J. C. Kissinger, A. J. M. Driessen, and M. Pohlschröder, “Identification of diverse archaeal proteins with class III signal peptides cleaved by distinct archaeal prepilin peptidases,” Journal of Bacteriology, vol. 189, no. 3, pp. 772–778, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. S.-O. Shan and P. Walter, “Co-translational protein targeting by the signal recognition particle,” FEBS Letters, vol. 579, no. 4, pp. 921–926, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. P. F. Egea, S.-O. Shan, J. Napetschnig, D. F. Savage, P. Walter, and R. M. Stroud, “Substrate twinning activates the signal recognition particle and its receptor,” Nature, vol. 427, no. 6971, pp. 215–221, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Haddad, R. W. Rose, and M. Pohlschröder, “The Haloferax volcanii FtsY homolog is critical for haloarchaeal growth but does not require the A domain,” Journal of Bacteriology, vol. 187, no. 12, pp. 4015–4022, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Tjalsma, A. Bolhuis, J. D. H. Jongbloed, S. Bron, and J. M. Van Dijl, “Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome,” Microbiology and Molecular Biology Reviews, vol. 64, no. 3, pp. 515–547, 2000. View at Google Scholar · View at Scopus
  57. J. L. Gardy, M. R. Laird, F. Chen et al., “PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis,” Bioinformatics, vol. 21, no. 5, pp. 617–623, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. J. D. Bendtsen, H. Nielsen, G. von Heijne, and S. Brunak, “Improved prediction of signal peptides: signalP 3.0,” Journal of Molecular Biology, vol. 340, no. 4, pp. 783–795, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. S. L. Bardy, J. Eichler, and K. F. Jarrell, “Archaeal signal peptides—a comparative survey at the genome level,” Protein Science, vol. 12, no. 9, pp. 1833–1843, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Abu-Qarn and J. Eichler, “An analysis of amino acid sequences surrounding archaeal glycoprotein sequons,” Archaea, vol. 2, no. 2, pp. 73–81, 2007. View at Google Scholar · View at Scopus
  61. M. Saleh, C. Song, S. Nasserulla, and L. G. Leduc, “Indicators from archaeal secretomes,” Microbiological Research, vol. 165, no. 1, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. P. G. Bagos, K. D. Tsirigos, S. K. Plessas, T. D. Liakopoulos, and S. J. Hamodrakas, “Prediction of signal peptides in archaea,” Protein Engineering, Design and Selection, vol. 22, no. 1, pp. 27–35, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. T. J. Williams, D. W. Burg, M. J. Raftery et al., “Global proteomic analysis of the insoluble, soluble, and supernatant fractions of the psychrophilic archaeon Methanococcoides burtonii part I: the effect of growth temperature,” Journal of Proteome Research, vol. 9, no. 2, pp. 640–652, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. D. R. Francoleon, P. Boontheung, Y. Yang et al., “S-layer, surface-accessible, and concanavalin a binding proteins of Methanosarcina acetivorans and Methanosarcina mazei,” Journal of Proteome Research, vol. 8, no. 4, pp. 1972–1982, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. L. Mashburn-Warren, R. J. C. Mclean, and M. Whiteley, “Gram-negative outer membrane vesicles: beyond the cell surface,” Geobiology, vol. 6, no. 3, pp. 214–219, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. N. Soler, E. Marguet, J.-M. Verbavatz, and P. Forterre, “Virus-like vesicles and extracellular DNA produced by hyperthermophilic archaea of the order Thermococcales,” Research in Microbiology, vol. 159, no. 5, pp. 390–399, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. A.-L. Reysenbach, Y. Liu, A. B. Banta et al., “A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents,” Nature, vol. 442, no. 7101, pp. 444–447, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. A. F. Ellen, S.-V. Albers, W. Huibers et al., “Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components,” Extremophiles, vol. 13, no. 1, pp. 67–79, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. R. Grimm, H. Singh, R. Rachel, D. Typke, W. Zillig, and W. Baumeister, “Electron tomography of ice-embedded prokaryotic cells,” Biophysical Journal, vol. 74, no. 2, pp. 1031–1042, 1998. View at Google Scholar · View at Scopus
  70. D. Prangishvili, I. Holz, E. Stieger, S. Nickell, J. K. Kristjansson, and W. Zillig, “Sulfolobicins, specific proteinaceous toxins produced by strains of the extremely thermophilic archaeal genus Sulfolobus,” Journal of Bacteriology, vol. 182, no. 10, pp. 2985–2988, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Y. Samson, T. Obita, S. M. Freund, R. L. Williams, and S. D. Bell, “A role for the ESCRT system in cell division in archaea,” Science, vol. 322, no. 5908, pp. 1710–1713, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. F. Mayer and G. Gottschalk, “The bacterial cytoskeleton and its putative role in membrane vesicle formation observed in a gram-positive bacterium producing starch-degrading enzymes,” Journal of Molecular Microbiology and Biotechnology, vol. 6, no. 3-4, pp. 127–132, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. M. L. Rodrigues, L. Nimrichter, D. L. Oliveira et al., “Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport,” Eukaryotic Cell, vol. 6, no. 1, pp. 48–59, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. B. L. Deatherage, J. C. Lara, T. Bergsbaken, S. L. R. Barrett, S. Lara, and B. T. Cookson, “Biogenesis of bacterial membrane vesicles,” Molecular Microbiology, vol. 72, no. 6, pp. 1395–1407, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. E.-Y. Lee, D.-S. Choi, K.-P. Kim, and Y. S. Gho, “Proteomics in Gram-negative bacterial outer membrane vesicles,” Mass Spectrometry Reviews, vol. 27, no. 6, pp. 535–555, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. C. Balsalobre, J. M. Silván, S. Berglund, Y. Mizunoe, B. E. Uhlin, and S. N. Wai, “Release of the type I secreted α-haemolysin via outer membrane vesicles from Escherichia coli,” Molecular Microbiology, vol. 59, no. 1, pp. 99–112, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. L. M. Mashburn and M. Whiteley, “Membrane vesicles traffic signals and facilitate group activities in a prokaryote,” Nature, vol. 437, no. 7057, pp. 422–425, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. A. J. McBroom and M. J. Kuehn, “Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response,” Molecular Microbiology, vol. 63, no. 2, pp. 545–558, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. N. A. Thomas, S. Mueller, A. Klein, and K. F. Jarrell, “Mutants in flaI and flaJ of the archaeon Methanococcus voltae are deficient in flagellum assembly,” Molecular Microbiology, vol. 46, no. 3, pp. 879–887, 2002. View at Publisher · View at Google Scholar · View at Scopus
  80. Z. Szabó, M. Sani, M. Groeneveld et al., “Flagellar motility and structure in the hyperthermoacidophilic archaeon Sulfolobus solfataricus,” Journal of Bacteriology, vol. 189, no. 11, pp. 4305–4309, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. S. L. Bardy, T. Mori, K. Komoriya, S.-I. Aizawa, and K. F. Jarrell, “Identification and localization of flagellins FlaA and FlaB3 within flagella of Methanococcus voltae,” Journal of Bacteriology, vol. 184, no. 19, pp. 5223–5233, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Nutsch, W. Marwan, D. Oesterhelt, and E. D. Gilles, “Signal processing and flagellar motor switching during phototaxis of Halobacterium salinarum,” Genome Research, vol. 13, no. 11, pp. 2406–2412, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Alam and D. Oesterhelt, “Morphology, function and isolation of halobacterial flagella,” Journal of Molecular Biology, vol. 176, no. 4, pp. 459–475, 1984. View at Google Scholar · View at Scopus
  84. D. J. Näther, R. Rachel, G. Wanner, and R. Wirth, “Flagella of Pyrococcus furiosus: multifunctional organelles, made for swimming, adhesion to various surfaces, and cell-cell contacts,” Journal of Bacteriology, vol. 188, no. 19, pp. 6915–6923, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Schopf, G. Wanner, R. Rachel, and R. Wirth, “An archaeal bi-species biofilm formed by Pyrococcus furiosus and Methanopyrus kandleri,” Archives of Microbiology, vol. 190, no. 3, pp. 371–377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. B. Zolghadr, A. Kling, A. Koerdt, A. J. M. Driessen, R. Rachel, and S.-V. Albers, “Appendage-mediated surface adherence of Sulfolobus solfataricus,” Journal of Bacteriology, vol. 192, no. 1, pp. 104–110, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Y. M. Ng, B. Chaban, and K. F. Jarrell, “Archaeal flagella, bacterial flagella and type IV pili: a comparison of genes and posttranslational modifications,” Journal of Molecular Microbiology and Biotechnology, vol. 11, no. 3–5, pp. 167–191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. S.-V. Albers and M. Pohlschröder, “Diversity of archaeal type IV pilin-like structures,” Extremophiles, vol. 13, no. 3, pp. 403–410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. S. Trachtenberg and S. Cohen-Krausz, “The archaeabacterial flagellar filament: a bacterial propeller with a pilus-like structure,” Journal of Molecular Microbiology and Biotechnology, vol. 11, no. 3–5, pp. 208–220, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. M. G. Pyatibratov, S. N. Beznosov, R. Rachel et al., “Alternative flagellar filament types in the haloarchaeon Haloarcula marismortui,” Canadian Journal of Microbiology, vol. 54, no. 10, pp. 835–844, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. L. Craig, M. E. Pique, and J. A. Tainer, “Type IV pilus structure and bacterial pathogenicity,” Nature Reviews Microbiology, vol. 2, no. 5, pp. 363–378, 2004. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Streif, W. F. Staudinger, W. Marwan, and D. Oesterhelt, “Flagellar rotation in the archaeon Halobacterium salinarum depends on ATP,” Journal of Molecular Biology, vol. 384, no. 1, pp. 1–8, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. N. A. Thomas, S. L. Bardy, and K. F. Jarrell, “The archaeal flagellum: a different kind of prokaryotic motility structure,” FEMS Microbiology Reviews, vol. 25, no. 2, pp. 147–174, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. S.-V. Albers and A. J. M. Driessen, “Analysis of ATPases of putative secretion operons in the thermoacidophilic archaeon Sulfolobus solfataricus,” Microbiology, vol. 151, no. 3, pp. 763–773, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. N. Patenge, A. Berendes, H. Engelhardt, S. C. Schuster, and D. Oesterhelt, “The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum,” Molecular Microbiology, vol. 41, no. 3, pp. 653–663, 2001. View at Publisher · View at Google Scholar · View at Scopus
  96. N. A. Thomas and K. F. Jarrell, “Characterization of flagellum gene families of methanogenic archaea and localization of novel flagellum accessory proteins,” Journal of Bacteriology, vol. 183, no. 24, pp. 7154–7164, 2001. View at Publisher · View at Google Scholar · View at Scopus
  97. Z. Szabó, S.-V. Albers, and A. J. M. Driessen, “Active-site residues in the type IV prepilin peptidase homologue PibD from the archaeon Sulfolobus solfataricus,” Journal of Bacteriology, vol. 188, no. 4, pp. 1437–1443, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Cohen-Krausz and S. Trachtenberg, “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,” Journal of Molecular Biology, vol. 321, no. 3, pp. 383–395, 2002. View at Publisher · View at Google Scholar · View at Scopus
  99. S. Cohen-Krausz and S. Trachtenberg, “The flagellar filament structure of the extreme acidothermophile Sulfolobus shibatae B12 suggests that archaeabacterial flagella have a unique and common symmetry and design,” Journal of Molecular Biology, vol. 375, no. 4, pp. 1113–1124, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. M. L. Kalmokoff and K. F. Jarrell, “Cloning and sequencing of a multigene family encoding the flagellins of Methanococcus voltae,” Journal of Bacteriology, vol. 173, no. 22, pp. 7113–7125, 1991. View at Google Scholar · View at Scopus
  101. B. Chaban, S. Y. M. Ng, M. Kanbe et al., “Systematic deletion analyses of the fla genes in the flagella operon identify several genes essential for proper assembly and function of flagella in the archaeon, Methanococcus maripaludis,” Molecular Microbiology, vol. 66, no. 3, pp. 596–609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. S. N. Beznosov, M. G. Pyatibratov, and O. V. Fedorov, “On the multicomponent nature of Halobacterium salinarum flagella,” Microbiology, vol. 76, no. 4, pp. 435–441, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. L. Gerl and M. Sumper, “Halobacterial flagellins are encoded by a multigene family. Characterization of five flagellin genes,” The Journal of Biological Chemistry, vol. 263, no. 26, pp. 13246–13251, 1988. View at Google Scholar · View at Scopus
  104. V. Y. Tarasov, M. G. Pyatibratov, S.-L. Tang, M. Dyall-Smith, and O. V. Fedorov, “Role of flagellins from A and B loci in flagella formation of Halobacterium salinarum,” Molecular Microbiology, vol. 35, no. 1, pp. 69–78, 2000. View at Publisher · View at Google Scholar · View at Scopus
  105. D. M. Faguy, D. P. Bayley, A. S. Kostyukova, N. A. Thomas, and K. F. Jarrell, “Isolation and characterization of flagella and flagellin proteins from the thermoacidophilic archaea Thermoplasma volcanium and Sulfolobus shibatae,” Journal of Bacteriology, vol. 178, no. 3, pp. 902–905, 1996. View at Google Scholar · View at Scopus
  106. S.-V. Albers, M. Jonuscheit, S. Dinkelaker et al., “Production of recombinant and tagged proteins in the hyperthermophilic archaeon Sulfolobus solfataricus,” Applied and Environmental Microbiology, vol. 72, no. 1, pp. 102–111, 2006. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Abendroth, P. Murphy, M. Sandkvist, M. Bagdasarian, and W. G. J. Hol, “The X-ray structure of the type II secretion system complex formed by the N-terminal domain of EpsE and the cytoplasmic domain of EpsL of Vibrio cholerae,” Journal of Molecular Biology, vol. 348, no. 4, pp. 845–855, 2005. View at Publisher · View at Google Scholar · View at Scopus
  108. M. Schlesner, A. Miller, S. Streif et al., “Identification of Archaea-specific chemotaxis proteins which interact with the flagellar apparatus,” BMC Microbiology, vol. 9, article 56, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. S. Nickell, R. Hegerl, W. Baumeister, and R. Rachel, “Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography,” Journal of Structural Biology, vol. 141, no. 1, pp. 34–42, 2003. View at Publisher · View at Google Scholar · View at Scopus
  110. G. Rieger, R. Rachel, R. Hermann, and K. O. Stetter, “Ultrastructure of the hyperthermophilic archaeon Pyrodictium-Abyssi,” Journal of Structural Biology, vol. 115, no. 1, pp. 78–87, 1995. View at Publisher · View at Google Scholar · View at Scopus
  111. C. Horn, B. Paulmann, G. Kerlen, N. Junker, and H. Huber, “In vivo observation of cell division of anaerobic hyperthermophiles by using a high-intensity dark-field microscope,” Journal of Bacteriology, vol. 181, no. 16, pp. 5114–5118, 1999. View at Google Scholar · View at Scopus
  112. K.O. Stetter, H. Konig, and E. Stackebrandt, “Pyrodictium gen-nov, a new genus of submarine disc-shaped sulfur reducing archaebacteria growing optimally at 105-degrees-C,” Systematic and Applied Microbiology, vol. 4, pp. 535–551, 1983. View at Google Scholar
  113. C. Moissl, R. Rachel, A. Briegel, H. Engelhardt, and R. Huber, “The unique structure of archaeal ‘hami’, highly complex cell appendages with nano-grappling hooks,” Molecular Microbiology, vol. 56, no. 2, pp. 361–370, 2005. View at Publisher · View at Google Scholar · View at Scopus
  114. C. Rudolph, G. Wanner, and R. Huber, “Natural communities of novel archaea and bacteria growing in cold sulfurous springs with a string-of-pearls-like morphology,” Applied and Environmental Microbiology, vol. 67, no. 5, pp. 2336–2344, 2001. View at Publisher · View at Google Scholar · View at Scopus
  115. D. W. Müller, C. Meyer, S. Gürster et al., “The Iho670 fibers of Ignicoccus hospitalis: a new type of archaeal cell surface appendage,” Journal of Bacteriology, vol. 191, no. 20, pp. 6465–6468, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. S. Fröls, M. Ajon, M. Wagner et al., “UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation,” Molecular Microbiology, vol. 70, no. 4, pp. 938–952, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. Y. A. Wang, X. Yu, S. Y. M. Ng, K. F. Jarrell, and E. H. Egelman, “The structure of an archaeal pilus,” Journal of Molecular Biology, vol. 381, no. 2, pp. 456–466, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. B. Zolghadr, S. Weber, Z. Szabó, A. J. M. Driessen, and S.-V. Albers, “Identification of a system required for the functional surface localization of sugar binding proteins with class III signal peptides in Sulfolobus solfataricus,” Molecular Microbiology, vol. 64, no. 3, pp. 795–806, 2007. View at Publisher · View at Google Scholar · View at Scopus
  119. D. F. Rodrigues and M. Elimelech, “Role of type 1 fimbriae and mannose in the development of Escherichia coli K12 biofilm: from initial cell adhesion to biofilm formation,” Biofouling, vol. 25, no. 5, pp. 401–411, 2009. View at Publisher · View at Google Scholar · View at Scopus
  120. H. Laue, A. Schenk, H. Li et al., “Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae,” Microbiology, vol. 152, no. 10, pp. 2909–2918, 2006. View at Publisher · View at Google Scholar · View at Scopus
  121. S. Tsuneda, H. Aikawa, H. Hayashi, A. Yuasa, and A. Hirata, “Extracellular polymeric substances responsible for bacterial adhesion onto solid surface,” FEMS Microbiology Letters, vol. 223, no. 2, pp. 287–292, 2003. View at Publisher · View at Google Scholar · View at Scopus