Table of Contents Author Guidelines Submit a Manuscript
International Journal of Microbiology
Volume 2010 (2010), Article ID 470138, 20 pages
http://dx.doi.org/10.1155/2010/470138
Review Article

Biosynthesis and Role of N-Linked Glycosylation in Cell Surface Structures of Archaea with a Focus on Flagella and S Layers

Department of Microbiology and Immunology, Queen's University, Kingston, ON, Canada K7L 3N6

Received 9 March 2010; Accepted 1 August 2010

Academic Editor: Charlene Kahler

Copyright © 2010 Ken F. Jarrell 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. 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
  2. C. M. Szymanski and B. W. Wren, “Protein glycosylation in bacterial mucosal pathogens,” Nature Reviews Microbiology, vol. 3, no. 3, pp. 225–237, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. M. F. Mescher and J. L. Strominger, “Purification and characterization of a prokaryotic glycoprotein from the cell envelope of Halobacterium salinarium,” Journal of Biological Chemistry, vol. 251, no. 7, pp. 2005–2014, 1976. View at Google Scholar · View at Scopus
  4. H. Magidovich and J. Eichler, “Glycosyltransferases and oligosaccharyltransferases in Archaea: putative components of the N-glycosylation pathway in the third domain of life,” FEMS Microbiology Letters, vol. 300, no. 1, pp. 122–130, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Messner, “Prokaryotic protein glycosylation is rapidly expanding from “curiosity” to “ubiquity”,” ChemBioChem, vol. 10, no. 13, pp. 2151–2154, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Schäffer and P. Messner, “Glycobiology of surface layer proteins,” Biochimie, vol. 83, no. 7, pp. 591–599, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Sumper, “Halobacterial glycoprotein biosynthesis,” Biochimica et Biophysica Acta, vol. 906, no. 1, pp. 69–79, 1987. View at Google Scholar · View at Scopus
  8. U. Karcher, H. Schroder, E. Haslinger et al., “Primary structure of the heterosaccharide of the surface glycoprotein of Methanothermus fervidus,” Journal of Biological Chemistry, vol. 268, no. 36, pp. 26821–26826, 1993. View at Google Scholar · View at Scopus
  9. S. Voisin, R. S. Houliston, J. Kelly et al., “Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae,” Journal of Biological Chemistry, vol. 280, no. 17, pp. 16586–16593, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Lechner and M. Sumper, “The primary structure of a procaryotic glycoprotein. Cloning and sequencing of the cell surface glycoprotein gene of halobacteria,” Journal of Biological Chemistry, vol. 262, no. 20, pp. 9724–9729, 1987. View at Google Scholar · View at Scopus
  11. R. Mengele and M. Sumper, “Drastic differences in glycosylation of related S-layer glycoproteins from moderate and extreme halophiles,” Journal of Biological Chemistry, vol. 267, no. 12, pp. 8182–8185, 1992. View at Google Scholar · View at Scopus
  12. M. Abu-Qarn, S. Yurist-Doutsch, A. Giordano et al., “Haloferax volcanii AglB and AglD are involved in N-glycosylation of the S-layer glycoprotein and proper assembly of the surface layer,” Journal of Molecular Biology, vol. 374, no. 5, pp. 1224–1236, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Kelly, S. M. Logan, K. F. Jarrell, D. J. VanDyke, and E. Vinogradov, “A novel N-linked flagellar glycan from Methanococcus maripaludis,” Carbohydrate Research, vol. 344, no. 5, pp. 648–653, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Wieland, G. Paul, and M. Sumper, “Halobacterial flagellins are sulfated glycoproteins,” Journal of Biological Chemistry, vol. 260, no. 28, pp. 15180–15185, 1985. View at Google Scholar · View at Scopus
  15. U. Zahringer, H. Moll, T. Hettmann, Y. A. Knirel, and G. Schafer, “Cytochrome b558/566 from the archaeon Sulfolobus acidocaldarius has a unique Asn-linked highly branched hexasaccharide chain containing 6-sulfoquinovose,” European Journal of Biochemistry, vol. 267, no. 13, pp. 4144–4149, 2000. View at Google Scholar
  16. L. L. Yang and A. Haug, “Purification and partial characterization of a procaryotic glycoprotein from the plasma membrane of Thermoplasma acidophilum,” Biochimica et Biophysica Acta, vol. 556, no. 2, pp. 265–277, 1979. View at Google Scholar · View at Scopus
  17. M. Igura, N. Maita, J. Kamishikiryo et al., “Structure-guided identification of a new catalytic motif of oligosaccharyltransferase,” EMBO Journal, vol. 27, no. 1, pp. 234–243, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Chaban, S. Voisin, J. Kelly, S. M. Logan, and K. F. Jarrell, “Identification of genes involved in the biosynthesis and attachment of Methanococcus voltae N-linked glycans: insight into N-linked glycosylation pathways in Archaea,” Molecular Microbiology, vol. 61, no. 1, pp. 259–268, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. D. J. Vandyke, J. Wu, S. M. Logan et al., “Identification of genes involved in the assembly and attachment of a novel flagellin N-linked tetrasaccharide important for motility in the archaeon Methanococcus maripaludis,” Molecular Microbiology, vol. 72, no. 3, pp. 633–644, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Abu-Qarn and J. Eichler, “Protein N-glycosylation in Archaea: defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation,” Molecular Microbiology, vol. 61, no. 2, pp. 511–525, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. H. J. Doddema, J. W. M. Derksen, and G. D. Vogels, “Fimbriae and flagella of methanogenic bacteria,” FEMS Microbiology Letters, vol. 5, no. 3, pp. 135–138, 1979. View at Publisher · View at Google Scholar · View at Scopus
  22. R. L. Weiss, “Attachment of bacteria to sulphur in extreme environments,” Journal of General Microbiology, vol. 77, no. 2, pp. 501–507, 1973. View at Google Scholar · View at Scopus
  23. 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
  24. 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
  25. T. Nutsch, D. Oesterhelt, E. D. Gilles, and W. Marwan, “A quantitative model of the switch cycle of an archaeal flagellar motor and its sensory control,” Biophysical Journal, vol. 89, no. 4, pp. 2307–2323, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. K. F. Jarrell and M. J. McBride, “The surprisingly diverse ways that prokaryotes move,” Nature Reviews Microbiology, vol. 6, no. 6, pp. 466–476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. 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
  28. S. L. Bardy, S. Y. M. Ng, and K. F. Jarrell, “Recent advances in the structure and assembly of the archaeal flagellum,” Journal of Molecular Microbiology and Biotechnology, vol. 7, no. 1-2, pp. 41–51, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. D. M. Faguy and K. F. Jarrell, “A twisted tale: the origin and evolution of motility and chemotaxis in prokaryotes,” Microbiology, vol. 145, no. 2, pp. 279–281, 1999. View at Google Scholar · View at Scopus
  30. 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
  31. 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
  32. K. F. Jarrell, D. P. Bayley, and A. S. Kostyukova, “The archaeal flagellum: a unique motility structure,” Journal of Bacteriology, vol. 178, no. 17, pp. 5057–5064, 1996. View at Google Scholar · View at Scopus
  33. 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
  34. 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
  35. 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
  36. L. Gerl and M. Sumper, “Halobacterial flagellins are encoded by a multigene family. Characterization of five flagellin genes,” Journal of Biological Chemistry, vol. 263, no. 26, pp. 13246–13251, 1988. View at Google Scholar · View at Scopus
  37. L. Gerl, R. Deutzmann, and M. Sumper, “Halobacterial flagellins are encoded by a multigene family. Identification of all five gene products,” FEBS Letters, vol. 244, no. 1, pp. 137–140, 1989. View at Google Scholar · View at Scopus
  38. 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
  39. I. Serganova, V. Ksenzenko, A. Serganov et al., “Sequencing of flagellin genes from Natrialba magadii provides new insight into evolutionary aspects of archaeal flagellins,” Journal of Bacteriology, vol. 184, no. 1, pp. 318–322, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Nagahisa, S. Ezaki, S. Fujiwara, T. Imanaka, and M. Takagi, “Sequence and transcriptional studies of five clustered flagellin genes from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1,” FEMS Microbiology Letters, vol. 178, no. 1, pp. 183–190, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. K. F. Jarrell, S. Y. Ng, and B. Chaban, “Flagellation and chemotaxis,” in Archaea: Molecular and Cellular Biology, R. Cavicchioli, Ed., pp. 385–410, ASM Press, Washington, DC, USA, 2007. View at Google Scholar
  42. 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
  43. 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
  44. 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
  45. D. M. Faguy, K. F. Jarrell, J. Kuzio, and M. L. Kalmokoff, “Molecular analysis of archaeal flagellins: similarity to the type IV pilin—transport superfamily widespread in bacteria,” Canadian Journal of Microbiology, vol. 40, no. 1, pp. 67–71, 1994. View at Google Scholar · View at Scopus
  46. 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
  47. S. L. Bardy and K. F. Jarrell, “Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae,” Molecular Microbiology, vol. 50, no. 4, pp. 1339–1347, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. D. P. Bayley and K. F. Jarrell, “Further evidence to suggest that archaeal flagella are related to bacterial type IV pili,” Journal of Molecular Evolution, vol. 46, no. 3, pp. 370–373, 1998. View at Google Scholar · View at Scopus
  49. C. R. Peabody, Y. J. Chung, M.-R. Yen, D. Vidal-Ingigliardi, A. P. Pugsley, and M. H. Saier Jr., “Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella,” Microbiology, vol. 149, no. 11, pp. 3051–3072, 2003. 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. 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
  52. 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
  53. 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
  54. N. A. Thomas, C. T. Pawson, and K. F. Jarrell, “Insertional inactivation of the flaH gene in the archaeon Methanococcus voltae results in non-flagellated cells,” Molecular Genetics and Genomics, vol. 265, no. 4, pp. 596–603, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. K. F. Jarrell, D. P. Bayley, V. Florian, and A. Klein, “Isolation and characterization of insertional mutations in flagellin genes in the archaeon Methanococcus voltae,” Molecular Microbiology, vol. 20, no. 3, pp. 657–666, 1996. View at Google Scholar · View at Scopus
  56. 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
  57. 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
  58. 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
  59. S. C. Kachlany, P. J. Planet, R. DeSalle, D. H. Fine, and D. H. Figurski, “Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum,” Trends in Microbiology, vol. 9, no. 9, pp. 429–437, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. 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
  61. R. M. Macnab, “Type III flagellar protein export and flagellar assembly,” Biochimica et Biophysica Acta, vol. 1694, no. 1–3, pp. 207–217, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. K. F. Jarrell, D. J. VanDyke, and J. Wu, “Archaeal flagella and pili,” in Pili and Flagella: Current Research and Future Trends, K. F. Jarrell, Ed., pp. 215–234, Caister Academic Press, Norfolk, UK, 2009. View at Google Scholar
  63. S. M. Logan, “Flagellar glycosylation—a new component of the motility repertoire?” Microbiology, vol. 152, no. 5, pp. 1249–1262, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. B. Chaban, S. M. Logan, J. F. Kelly, and K. F. Jarrell, “AglC and AglK are involved in biosynthesis and attachment of diacetylated glucuronic acid to the N-glycan in Methanococcus voltae,” Journal of Bacteriology, vol. 91, no. 1, pp. 187–195, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Thoma, M. Frank, R. Rachel et al., “The Mth60 fimbriae of Methanothermobacter thermoautotrophicus are functional adhesins,” Environmental Microbiology, vol. 10, no. 10, pp. 2785–2795, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Fröls, P. M. K. Gordon, M. A. Panlilio et al., “Response of the hyperthermophilic archaeon Sulfolobus solfataricus to UV damage,” Journal of Bacteriology, vol. 189, no. 23, pp. 8708–8718, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. 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
  68. 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
  69. 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
  70. S. Y. M. Ng, D. J. VanDyke, B. Chaban et al., “Different minimal signal peptide lengths recognized by the archaeal prepilin-like peptidases FlaK and PibD,” Journal of Bacteriology, vol. 191, no. 21, pp. 6732–6740, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. 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
  72. 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
  73. 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
  74. R. Henneberger, C. Moissl, T. Amann, C. Rudolph, and R. Huber, “New insights into the lifestyle of the cold-loving SM1 euryarchaeon: natural growth as a monospecies biofilm in the subsurface,” Applied and Environmental Microbiology, vol. 72, no. 1, pp. 192–199, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. 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
  76. 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
  77. M. G. L. Elferink, S.-V. Albers, W. N. Konings, and A. J. M. Driessen, “Sugar transport in Sulfolobus solfataricus is mediated by two families of binding protein-dependent ABC transporters,” Molecular Microbiology, vol. 39, no. 6, pp. 1494–1503, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. 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
  79. M. L. Kalmokoff, S. F. Koval, and K. F. Jarrell, “Relatedness of the flagellins from methanogens,” Archives of Microbiology, vol. 157, no. 6, pp. 481–487, 1992. View at Google Scholar · View at Scopus
  80. H. Claus, E. Akça, T. Debaerdemaeker et al., “Molecular organization of selected prokaryotic S-layer proteins,” Canadian Journal of Microbiology, vol. 51, no. 9, pp. 731–743, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. H. Engelhardt, “Are S-layers exoskeletons? The basic function of protein surface layers revisited,” Journal of Structural Biology, vol. 160, no. 2, pp. 115–124, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Messner, “Bacterial glycoproteins,” Glycoconjugate Journal, vol. 14, no. 1, pp. 3–11, 1997. View at Publisher · View at Google Scholar · View at Scopus
  83. P. Messner, G. Allmaier, C. Schäffer et al., “Biochemistry of S-layers,” FEMS Microbiology Reviews, vol. 20, no. 1-2, pp. 25–46, 1997. View at Publisher · View at Google Scholar · View at Scopus
  84. U. B. Sleytr and T. J. Beveridge, “Bacterial S-layers,” Trends in Microbiology, vol. 7, no. 6, pp. 253–260, 1999. View at Publisher · View at Google Scholar · View at Scopus
  85. R. K. Upreti, M. Kumar, and V. Shankar, “Bacterial glycoproteins: functions, biosynthesis and applications,” Proteomics, vol. 3, no. 4, pp. 363–379, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. D. Pum, P. Messner, and U. B. Sleytr, “Role of the S layer in morphogenesis and cell division of the archaebacterium Methanocorpusculum sinense,” Journal of Bacteriology, vol. 173, no. 21, pp. 6865–6873, 1991. View at Google Scholar · View at Scopus
  87. M. Sára and U. B. Sleytr, “S-layer proteins,” Journal of Bacteriology, vol. 182, no. 4, pp. 859–868, 2000. View at Publisher · View at Google Scholar · View at Scopus
  88. B. M. Phipps, R. Huber, and W. Baumeister, “The cell envelope of the hyperthermophilic archaebacterium Pyrobaculum organotrophum consists of two regularly arrayed protein layers: three-dimensional structure of the outer layer,” Molecular Microbiology, vol. 5, no. 2, pp. 253–265, 1991. View at Google Scholar · View at Scopus
  89. M. Wacker, D. Linton, P. G. Hitchen et al., “N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli,” Science, vol. 298, no. 5599, pp. 1790–1793, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. H. Nothaft, X. Liu, D. J. McNally, and C. M. Szymanski, “N-linked protein glycosylation in a bacterial system,” Methods in Molecular Biology, vol. 600, pp. 227–243, 2010. View at Google Scholar · View at Scopus
  91. N. Maita, J. Nyirenda, M. Igura, J. Kamishikiryo, and D. Kohda, “Comparative structural biology of eubacterial and archaeal oligosaccharyltransferases,” Journal of Biological Chemistry, vol. 285, no. 7, pp. 4941–4950, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Linton, N. Dorrell, P. G. Hitchen et al., “Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway,” Molecular Microbiology, vol. 55, no. 6, pp. 1695–1703, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. J. Lechner, F. Wieland, and M. Sumper, “Biosynthesis of sulfated saccharides N-glycosidically linked to the protein via glucose. Purification and identification of sulfated dolichyl monophosphoryl tetrasaccharides from halobacteria,” Journal of Biological Chemistry, vol. 260, no. 2, pp. 860–866, 1985. View at Google Scholar · View at Scopus
  94. C. Kuntz, J. Sonnenbichler, I. Sonnenbichler, M. Sumper, and R. Zeitler, “Isolation and characterization of dolichol-linked oligoscaccharides from Haloferax volcanii,” Glycobiology, vol. 7, no. 7, pp. 897–904, 1997. View at Publisher · View at Google Scholar · View at Scopus
  95. E. Weerapana and B. Imperiali, “Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems,” Glycobiology, vol. 16, no. 6, pp. 91R–101R, 2006. View at Publisher · View at Google Scholar · View at Scopus
  96. J. Lechner and F. Wieland, “Structure and biosynthesis of prokaryotic glycoproteins,” Annual Review of Biochemistry, vol. 58, pp. 173–194, 1989. View at Google Scholar · View at Scopus
  97. J. Kelly, H. Jarrell, L. Millar et al., “Biosynthesis of the N-linked glycan in Campylobacter jejuni and addition onto protein through block transfer,” Journal of Bacteriology, vol. 188, no. 7, pp. 2427–2434, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. J. Helenius, D. T. W. Ng, C. L. Marolda, P. Walter, M. A. Valvano, and M. Aebi, “Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein,” Nature, vol. 415, no. 6870, pp. 447–450, 2002. View at Publisher · View at Google Scholar · View at Scopus
  99. C. G. Frank, S. Sanyal, J. S. Rush, C. J. Waechter, and A. K. Menon, “Does Rft1 flip an N-glycan lipid precursor?” Nature, vol. 454, no. 7204, pp. E3–E4, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. N. Plavner and J. Eichler, “Defining the topology of the N-glycosylation pathway in the halophilic archaeon Haloferax volcanii,” Journal of Bacteriology, vol. 190, no. 24, pp. 8045–8052, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. N. M. Young, J.-R. Brisson, J. Kelly et al., “Structure of the N-linked glycan present on multiple glycoproteins in the gram-negative bacterium, Campylobacter jejuni,” Journal of Biological Chemistry, vol. 277, no. 45, pp. 42530–42539, 2002. View at Publisher · View at Google Scholar · View at Scopus
  102. P. Messner and U. B. Sleytr, “Asparaginyl-rhamnose: a novel type of protein-carbohydrate linkage in a eubacterial surface-layer glycoprotein,” FEBS Letters, vol. 228, no. 2, pp. 317–320, 1988. View at Google Scholar · View at Scopus
  103. C. Schäffer, T. Wugeditsch, H. Kählig, A. Scheberl, S. Zayni, and P. Messner, “The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation,” Journal of Biological Chemistry, vol. 277, no. 8, pp. 6230–6239, 2002. View at Publisher · View at Google Scholar · View at Scopus
  104. R. Schreiner, E. Schnabel, and F. Wieland, “Novel N-glycosylation in eukaryotes: laminin contains the linkage unit β- glucosylasparagine,” Journal of Cell Biology, vol. 124, no. 6, pp. 1071–1081, 1994. View at Google Scholar · View at Scopus
  105. F. Wieland, R. Heitzer, and W. Schaefer, “Asparaginylglucose: novel type of carbohydrate linkage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 80, no. 181, pp. 5470–5474, 1983. View at Google Scholar · View at Scopus
  106. M. Abu-Qarn, J. Eichler, and N. Sharon, “Not just for Eukarya anymore: protein glycosylation in Bacteria and Archaea,” Current Opinion in Structural Biology, vol. 18, no. 5, pp. 544–550, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. M. Wacker, M. F. Feldman, N. Callewaert et al., “Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 7088–7093, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. V. W.-F. Tai and B. Imperiali, “Substrate specificity of the glycosyl donor for oligosaccharyl transferase,” Journal of Organic Chemistry, vol. 66, no. 19, pp. 6217–6228, 2001. View at Publisher · View at Google Scholar · View at Scopus
  109. M. F. Feldman, M. Wacker, M. Hernandez et al., “Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 8, pp. 3016–3021, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. D. Karaoglu, D. J. Kelleher, and R. Gilmore, “Allosteric regulation provides a molecular mechanism for preferential utilization of the fully assembled dolichol-linked oligosaccharide by the yeast oligosaccharyltransferase,” Biochemistry, vol. 40, no. 40, pp. 12193–12206, 2001. View at Publisher · View at Google Scholar · View at Scopus
  111. P. Burda and M. Aebi, “The ALG10 locus of Saccharomyces cerevisiae encodes the α-1,2 glucosyltransferase of the endoplasmic reticulum: the terminal glucose of the lipid-link oligosaccharide is required for efficient N-linked glycosylation,” Glycobiology, vol. 8, no. 5, pp. 455–462, 1998. View at Publisher · View at Google Scholar · View at Scopus
  112. M. Nita-Lazar, M. Wacker, B. Schegg, S. Amber, and M. Aebi, “The N-X-S/T consensus sequence is required but not sufficient for bacterial N-linked protein glycosylation,” Glycobiology, vol. 15, no. 4, pp. 361–367, 2005. View at Publisher · View at Google Scholar · View at Scopus
  113. 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
  114. R. Zeitler, E. Hochmuth, R. Deutzmann, and M. Sumper, “Exchange of Ser-4 for Val, Leu or Asn in the sequon Asn-Ala-Ser does not prevent N-glycosylation of the cell surface glycoprotein from Halobacterium halobium,” Glycobiology, vol. 8, no. 12, pp. 1157–1164, 1998. View at Publisher · View at Google Scholar · View at Scopus
  115. H. Magidovich, S. Yurist-Doutsch, Z. Konrad et al., “AglP is a S-adenosyl-L-methionine-dependent methyltransferase that participates in the N-glycosylation pathway of Haloferax volcanii,” Molecular Microbiology, vol. 76, no. 1, pp. 190–199, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Sumper and F. T. Wieland, “Bacterial glycoproteins,” in Glycoproteins, J. Montreuil, J. F. G. Vliegenthart, and H. Schachter, Eds., pp. 455–473, Elsevier, Amsterdam, The Netherlands, 1995. View at Google Scholar
  117. P. Pellerin, B. Fournet, and P. Debeire, “Evidence for the glycoprotein nature of the cell sheath of Methanosaeta-like cells in the culture of Methanothrix soehngenii strain FE,” Canadian Journal of Microbiology, vol. 36, no. 9, pp. 631–636, 1990. View at Google Scholar · View at Scopus
  118. H. Shams-Eldin, B. Chaban, S. Niehus, R. T. Schwarz, and K. F. Jarrell, “Identification of the archaeal alg7 gene homolog (encoding N-acetylglucosamine-1-phosphate transferase) of the N-linked glycosylation system by cross-domain complementation in Saccharomyces cerevisiae,” Journal of Bacteriology, vol. 190, no. 6, pp. 2217–2220, 2008. View at Publisher · View at Google Scholar · View at Scopus
  119. S. C. Namboori and D. E. Graham, “Acetamido sugar biosynthesis in the euryarchaea,” Journal of Bacteriology, vol. 190, no. 8, pp. 2987–2996, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. F. D. Sauer, B. A. Blackwell, J. K. G. Kramer, and B. J. Marsden, “Structure of novel cofactor containing N-(7-mercaptoheptanoyl)-O-3-phosphothreonine,” Biochemistry, vol. 29, no. 33, pp. 7593–7600, 1990. View at Publisher · View at Google Scholar · View at Scopus
  121. B. C. Moore and J. A. Leigh, “Markerless mutagenesis in Methanococcus maripaludis demonstrates roles for alanine dehydrogenase, alanine racemase, and alanine permease,” Journal of Bacteriology, vol. 187, no. 3, pp. 972–979, 2005. View at Publisher · View at Google Scholar · View at Scopus
  122. J. S. Rush, C. Alaimo, R. Robbiani, M. Wacker, and C. J. Waechter, “A novel epimerase that converts GlcNAc-P-P-undecaprenol to GalNAc-P-P-undecaprenol in Escherichia coli O1570,” Journal of Biological Chemistry, vol. 285, no. 3, pp. 1671–1680, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. G. Ferrante, I. Ekiel, and G. D. Sprott, “Structural characterization of the lipids of Methanococcus voltae, including a novel N-acetylglucosamine 1-phosphate diether,” Journal of Biological Chemistry, vol. 261, no. 36, pp. 17062–17066, 1986. View at Google Scholar · View at Scopus
  124. S. Yurist-Doutsch and J. Eichler, “Manual annotation, transcriptional analysis, and protein expression studies reveal novel genes in the agl cluster responsible for N glycosylation in the halophilic archaeon Haloferax volcanii,” Journal of Bacteriology, vol. 191, no. 9, pp. 3068–3075, 2009. View at Publisher · View at Google Scholar · View at Scopus
  125. S. Yurist-Doutsch, H. Magidovich, V. V. Ventura, P. G. Hitchen, A. Dell, and J. Eichler, “N-glycosylation in Archaea: on the coordinated actions of Haloferax volcanii AglF and AglM,” Molecular Microbiology, vol. 75, no. 4, pp. 1047–1058, 2010. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Yurist-Doutsch, M. Abu-Qarn, F. Battaglia et al., “AglF, aglG and aglI, novel members of a gene island involved in the N-glycosylation of the Haloferax volcanii S-layer glycoprotein,” Molecular Microbiology, vol. 69, no. 5, pp. 1234–1245, 2008. View at Publisher · View at Google Scholar · View at Scopus
  127. M. Abu-Qarn, A. Giordano, F. Battaglia et al., “Identification of AglE, a second glycosyltransferase involved in N glycosylation of the Haloferax volcanii S-layer glycoprotein,” Journal of Bacteriology, vol. 190, no. 9, pp. 3140–3146, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. D. J. VanDyke, J. Wu, S. Y. M. Ng et al., “Identification of a putative acetyltransferase gene, MMP0350, which affects proper assembly of both flagella and pili in the archaeon Methanococcus maripaludis,” Journal of Bacteriology, vol. 190, no. 15, pp. 5300–5307, 2008. View at Publisher · View at Google Scholar · View at Scopus
  129. M. Igura, N. Maita, T. Obita, J. Kamishikiryo, K. Maenaka, and D. Kohda, “Purification, crystallization and preliminary X-ray diffraction studies of the soluble domain of the oligosaccharyltransferase STT3 subunit from the thermophilic archaeon Pyrococcus furiosus,” Acta Crystallographica F, vol. 63, no. 9, pp. 798–801, 2007. View at Publisher · View at Google Scholar · View at Scopus
  130. D. P. Bayley, M. L. Kalmokoff, and K. F. Jarrell, “Effect of bacitracin on flagellar assembly and presumed glycosylation of the flagellins of Methanococcus deltae,” Archives of Microbiology, vol. 160, no. 3, pp. 179–185, 1993. View at Google Scholar · View at Scopus
  131. D. E. Bradley, “A function of Pseudomonas aeruginosa PAO polar pili: twitching motility,” Canadian Journal of Microbiology, vol. 26, no. 2, pp. 146–154, 1980. View at Google Scholar · View at Scopus
  132. M. Pohlschröder, M. I. Giménez, and K. F. Jarrell, “Protein transport in Archaea: sec and twin arginine translocation pathways,” Current Opinion in Microbiology, vol. 8, no. 6, pp. 713–719, 2005. View at Publisher · View at Google Scholar · View at Scopus
  133. M. S. Strom, D. N. Nunn, and S. Lory, “Posttranslational processing of type IV prepilin and homologs by PilD of Pseudomonas aeruginosa,” Methods in Enzymology, vol. 235, pp. 527–540, 1994. View at Publisher · View at Google Scholar · View at Scopus
  134. Y. Y. Polosina, K. F. Jarrell, O. V. Fedorov, and A. S. Kostyukova, “Nucleoside diphosphate kinase from haloalkaliphilic archaeon Natronobacterium magadii: purification and characterization,” Extremophiles, vol. 2, no. 3, pp. 333–338, 1998. View at Publisher · View at Google Scholar · View at Scopus
  135. C. Schäffer and P. Messner, “Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology,” Glycobiology, vol. 14, no. 8, pp. 31R–42R, 2004. View at Publisher · View at Google Scholar · View at Scopus
  136. S. Yurist-Doutsch, B. Chaban, D. J. VanDyke, K. F. Jarrell, and J. Eichler, “Sweet to the extreme: protein glycosylation in Archaea,” Molecular Microbiology, vol. 68, no. 5, pp. 1079–1084, 2008. View at Publisher · View at Google Scholar · View at Scopus