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

Volumn 72, Issue 3, 2009, Pages 633-644

  Vandyke, David J ^a   Wu, John ^a   Logan, Susan M ^b   Kelly, John F ^b   Mizuno, Shino ^c   Aizawa, Shin Ichi ^c   Jarrell, Ken F ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c PREFECTURAL UNIVERSITY OF HIROSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; GLYCAN; GLYCOSYLTRANSFERASE; N LINKED TETRASACCHARIDE; OLIGOSACCHARYLTRANSFERASE; TETRASACCHARIDE; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE DELETION; GENE IDENTIFICATION; IMMUNOBLOTTING; MASS SPECTROMETRY; METHANOCOCCUS MARIPALUDIS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE;

ARCHAEAL PROTEINS; FLAGELLIN; GENE DELETION; GENES, ARCHAEAL; GLYCOSYLTRANSFERASES; HEXOSYLTRANSFERASES; MEMBRANE PROTEINS; METHANOCOCCUS; POLYSACCHARIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL;

ARCHAEA; METHANOCOCCUS MARIPALUDIS;

EID: 65349147066     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06671.x     Document Type: Article

References (43)

1. Abu-Qarn, M. Eichler, J. (2007) An analysis of amino acid sequences surrounding archaeal glycoprotein sequons. Archaea 2 : 73 81.
2. Abu-Qarn, M., Yurist-Doutsch, S., Giordano, A., Trauner, A., Morris, H.R., Hitchen, P., et al. (2007) Haloferax volcanii AglB and AglD are involved in N-glycosylation of the S-layer glycoprotein and proper assembly of the surface layer. J Mol Biol 374 : 1224 1236.
3. Abu-Qarn, M., Giordano, A., Battaglia, F., Trauner, A., Hitchen, P.G., Morris, H.R., et al. (2008) Identification of AglE, a second glycosyltransferase involved in N-glycosylation of the Haloferax volcanii S-layer glycoprotein. J Bacteriol 190 : 3140 3146.
4. Balch, W.E., Fox, G.E., Magrum, L.J., Woese, C.R. Wolfe, R.S. (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43 : 260 296.
5. Bardy, S.L., Mori, T., Komoriya, K., Aizawa, S.-I. Jarrell, K.F. (2002) Identification and localization of flagellins FlaA and FlaB3 within flagella of Methanococcus voltae. J Bacteriol 184 : 5223 5233.
6. Blank, C.E., Kessler, P.S. Leigh, J.A. (1995) Genetics in methanogens: transposon insertion mutagenesis of a Methanococcus maripaludis nifH gene. J Bacteriol 177 : 5773 5777.
7. Chaban, B., Voisin, S., Kelly, J., Logan, S.M. Jarrell, K.F. (2006) Identification of genes involved in the biosynthesis and attachment of Methanococcus voltae N-linked glycans: insight into N-linked glycosylation pathways in archaea. Mol Microbiol 61 : 259 268.
8. Chaban, B., Ng, S.Y., Kanbe, M., Saltzman, I., Nimmo, G., Aizawa, S.I. Jarrell, K.F. (2007) 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. Mol Microbiol 66 : 596 609.
9. Chaban, B., Logan, S.M., Kelly, J.F. Jarrell, K.F. (2009) AglC and AglK are involved in biosynthesis and attachment of diacetylated glucuronic acid to the N-glycan in Methanococcus voltae. J Bacteriol 191 : 187 195.
10. Cohen-Krausz, S. Trachtenberg, S. (2008) The flagellar filament structure of the extreme acidothermophile Sulfolobus shibatae B12 suggests that archaeabacterial flagella have a unique and common symmetry and design. J Mol Biol 375 : 1113 1124.
11. Eichler, J. Adams, M.W.W. (2005) Posttranslational protein modification in archaea. Microbiol Mol Biol Rev 69 : 393 425.
12. Gavel, Y. von Heijne, G. (1990) Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng 3 : 433 442.
13. Goon, S., Kelly, J.F., Logan, S.M., Ewing, C.P. Guerry, P. (2003) Pseudaminic acid, the major modification on Campylobacter flagellin, is synthesized via the Cj1293 gene. Mol Microbiol 50 : 659 671.
14. Jarrell, K.F. McBride, M.J. (2008) The surprisingly diverse ways that prokaryotes move. Nat Rev Microbiol 6 : 466 476.
15. Jarrell, K.F., Ng, S.Y. Chaban, B. (2007) Flagellation and chemotaxis. In Archaea: Molecular and Cellular Biology. Cavicchioli, R. (ed.). Washington, DC : American Society for Microbiology Press, pp. 385 410.
16. Kelly, J., Logan, S.M., Jarrell, K.F., Vandyke, D.J. Vinogradov, E. (2009) A novel N-linked flagellar glycan from Methanococcus maripaludis. Carbohydr Res 344 : 648 653.
17. Kessler, P.S. Leigh, J.A. (1999) Genetics of nitrogen regulation in Methanococcus maripaludis. Genetics 152 : 1343 1351.
18. Kowarik, M., Young, N.M., Numao, S., Schulz, B.L., Hug, I., Callewaert, N., et al. (2006) Definition of the bacterial N-glycosylation site consensus sequence. EMBO J 25 : 1957 1966.
19. Leclerc, G., Wang, S.P. Ely, B. (1998) A new class of Caulobacter crescentus flagellar genes. J Bacteriol 180 : 5010 5019.
20. Lie, T.J., Wood, G.E. Leigh, J.A. (2005) Regulation of nif expression in Methanococcus maripaludis: roles of the euryarchaeal repressor NrpR, 2-oxoglutarate, and two operators. J Biol Chem 280 : 5236 5241.
21. Logan, S.M. (2006) Flagellar glycosylation - a new component of the motility repertoire? Microbiology 152 : 1249 1262.
22. Macnab, R.M. (2003) How bacteria assemble flagella. Annu Rev Microbiol 57 : 77 100.
23. Moore, B.C. Leigh, J.A. (2005) Markerless mutagenesis in Methanococcus maripaludis demonstrates roles for alanine dehydrogenase, alanine racemase, and alanine permease. J Bacteriol 187 : 972 979.
24. Namboori, S.C. Graham, D.E. (2008) Acetamido sugar biosynthesis in the euryarchaea. J Bacteriol 190 : 2987 2996.
25. Ng, S.Y., Chaban, B. Jarrell, K.F. (2006) Archaeal flagella, bacterial flagella and type IV pili: a comparison of genes and posttranslational modifications. J Mol Microbiol Biotechnol 11 : 167 191.
26. Peabody, C.R., Chung, Y.J., Yen, M.R., Vidal-Ingigliardi, D., Pugsley, A.P. Saier, M.H., Jr, (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149 : 3051 3072.
27. Plavner, N. Eichler, J. (2008) Defining the topology of the N-glycosylation pathway in the halophilic archaeon Haloferax volcanii. J Bacteriol 190 : 8045 8052.
28. Schirm, M., Soo, E.C., Aubry, A.J., Austin, J., Thibault, P. Logan, S.M. (2003) Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori. Mol Microbiol 48 : 1579 1592.
29. Schirm, M., Arora, S.K., Verma, A., Vinogradov, E., Thibault, P., Ramphal, R. Logan, S.M. (2004a) Structural and genetic characterization of glycosylation of type a flagellin in Pseudomonas aeruginosa. J Bacteriol 186 : 2523 2531.
30. Schirm, M., Kalmokoff, M., Aubry, A., Thibault, P., Sandoz, M. Logan, S.M. (2004b) Flagellin from Listeria monocytogenes is glycosylated with beta-O-linked N-acetylglucosamine. J Bacteriol 186 : 6721 6727.
31. Shams-Eldin, H., Chaban, B., Niehus, S., Schwarz, R.T. Jarrell, K.F. (2008) 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. J Bacteriol 190 : 2217 2220.
32. Shen, A., Kamp, H.D., Grundling, A. Higgins, D.E. (2006) A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev 20 : 3283 3295.
33. Sumper, M. (1987) Halobacterial glycoprotein biosynthesis. Biochim Biophys Acta 906 : 69 79.
34. Szymanski, C.M. Wren, B.W. (2005) Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3 : 225 237.
35. Takeuchi, K., Taguchi, F., Inagaki, Y., Toyoda, K., Shiraishi, T. Ichinose, Y. (2003) Flagellin glycosylation island in Pseudomonas syringae pv. glycinea and its role in host specificity. J Bacteriol 185 : 6658 6665.
36. Trachtenberg, S. Cohen-Krausz, S. (2006) The archaeabacterial flagellar filament: a bacterial propeller with a pilus-like structure. J Mol Microbiol Biotechnol 11 : 208 220.
37. Twine, S.M., Paul, C.J., Vinogradov, E., McNally, D.J., Brisson, J.R., Mullen, J.A., et al. (2008) Flagellar glycosylation in Clostridium botulinum. FEBS J 275 : 4428 4444.
38. VanDyke, D.J., Wu, J., Ng, S.Y., Kanbe, M., Chaban, B., Aizawa, S.I. Jarrell, K.F. (2008) Identification of putative acetyltransferase gene, MMP0350, which affects proper assembly of both flagella and pili in the archaeon Methanococcus maripaludis. J Bacteriol 190 : 5300 5307.
39. Voisin, S., Houliston, R.S., Kelly, J., Brisson, J.R., Watson, D., Bardy, S.L., et al. (2005) Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae. J Biol Chem 280 : 16586 16593.
40. Weerapana, E. Imperiali, B. (2006) Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16 : 91R 101R.
41. Wieland, F. (1988) Structure and biosynthesis of prokaryotic glycoproteins. Biochimie 70 : 1493 1504.
42. Yurist-Doutsch, S., Chaban, B., VanDyke, D.J., Jarrell, K.F. Eichler, J. (2008a) Sweet to the extreme: protein glycosylation in archaea. Mol Microbiol 68 : 1079 1084.
43. Yurist-Doutsch, S., Abu-Qarn, M., Battaglia, F., Morris, H.R., Hitchen, P.G., Dell, A. Eichler, J. (2008b) AglF, aglG and aglI, novel members of a gene island involved in the N-glycosylation of the Haloferax volcanii S-layer glycoprotein. Mol Microbiol 69 : 1234 1245.