Comparative genomics analysis of completely sequenced microbial genomes reveals the ubiquity of N-linked glycosylation in prokaryotes

Molecular BioSystems

Volumn 7, Issue 5, 2011, Pages 1629-1645

  Kumar, Manjeet ^a   Balaji, Petety V ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPYLOBACTER JEJUNI; PROKARYOTA;

EID: 79954452580     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c0mb00259c     Document Type: Article

References (97)

1. S. Okuda G. Weinbaum An envelope-specific glycoprotein from Escherichia coli B Biochemistry 1968 7 2819 2825
2. M. F. Mescher J. L. Strominger S. W. Watson Protein and carbohydrate composition of the cell envelope of Halobacterium salinarium J. Bacteriol. 1974 120 945 954
3. S. Moens K. Michiels J. Vanderleyden Glycosylation of the flagellin of the polar flagellum of Azospirillum brasilense, a Gram-negative nitrogen-fixing bacterium Microbiology 1995 141 2651 2657
4. F. E. Aas A. Vik J. Vedde M. Koomey W. Egge-Jacobsen Neisseria gonorrhoeae O-linked pilin glycosylation: functional analyses define both the biosynthetic pathway and glycan structure Mol. Microbiol. 2007 65 607 624 (Pubitemid 47077225)
5. P. M. Power L. F. Roddam M. Dieckelmann Y. N. Srikhanta Y. C. Tan A. W. Berrington M. P. Jennings Genetic characterization of pilin glycosylation in Neisseria meningitidis Microbiology 2000 146 967 979 (Pubitemid 30201044)
6. P. M. Power L. F. Roddam K. Rutter S. Z. Fitzpatrick Srikhanta M. P. Jennings Genetic characterization of pilin glycosylation and phase variation in Neisseria meningitidis Mol. Microbiol. 2003 49 833 847 (Pubitemid 36918700)
7. E. Stimson M. Virji K. Makepeace et al. (11 co-authors), Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6- trideoxyhexose Mol. Microbiol. 1995 17 1201 1214
8. P. Castric PilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin Microbiology 1995 141 1247 1254
9. A. Faridmoayer M. A. Fentabil D. C. Mills J. S. Klassen M. F. Feldman Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation J. Bacteriol. 2007 189 8088 8098 (Pubitemid 350178920)
10. D. Linton N. Dorrell P. G. Hitchen S. Amber A. V. Karlyshev H. R. Morris A. Dell M. A. Valvano M. Aebi B. W. Wren Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway Mol. Microbiol. 2005 55 1695 1703 (Pubitemid 40445207)
11. C. M. Szymanski R. Yao C. P. Ewing T. J. Trust P. Guerry Evidence for a system of general protein glycosylation in Campylobacter jejuni Mol. Microbiol. 1999 32 1022 1030 (Pubitemid 29255768)
12. C. M. Szymanski S. M. Logan D. Linton B. W. Wren Campylobacter - a tale of two protein glycosylation systems Trends Microbiol. 2003 11 233 238 (Pubitemid 36645007)
13. S. Grass A. Z. Buscher W. E. Swords M. A. Apicella S. J. Barenkamp N. Ozchlewski J. W. St Geme, III The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis Mol. Microbiol. 2003 48 737 751 (Pubitemid 36819059)
14. M. Schirm E. C. Soo A. J. Aubry J. Austin P. Thibault S. M. Logan Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori Mol. Microbiol. 2003 48 1579 1592 (Pubitemid 36751063)
15. S. Yurist-Doutsch 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 J. Bacteriol. 2009 191 3068 3075
16. C. M. Fletcher M. J. Coyne O. F. Villa M. Chatzidaki-Livanis L. E. Comstock A general O-glycosylation system important to the physiology of a major human intestinal symbiont Cell 2009 137 321 331
17. M. Abu-Qarn J. Eichler N. Sharon Not just for eukarya anymore: protein glycosylation in bacteria and archaea Curr. Opin. Struct. Biol. 2008 8 544 550
18. D. Calo L. Kaminski J. Eichler Protein glycosylation in archaea: sweet and extreme Glycobiology 2010 20 1065 1076
19. P. Messner Bacterial glycoproteins Glycoconjugate J. 1997 14 3 11 (Pubitemid 27104489)
20. R. K. Upreti M. Kumar V. Shankar Bacterial glycoproteins: functions, biosynthesis and applications Proteomics 2003 3 363 379 (Pubitemid 36428290)
21. S. Yurist-Doutsch B. Chaban D. J. VanDyke K. F. Jarrell J. Eichler Sweet to the extreme: protein glycosylation in Archaea Mol. Microbiol. 2008 68 1079 1084 (Pubitemid 351670196)
22. S. Moens J. Vanderleyden Glycoproteins in prokaryotes Arch. Microbiol. 1997 168 169 175 (Pubitemid 27394182)
23. A. Vik F. E. Aas J. H. Anonsen S. Bilsborough A. Schneider W. Egge-Jacobsen M. Koomey Broad spectrum O-linked protein glycosylation in the human pathogen Neisseria gonorrhoeae Proc. Natl. Acad. Sci. U. S. A. 2009 106 4447 4452
24. N. M. Young J.-R. Brisson J. Kelly D. C. Watson L. Tessier P. H. Lanthier H. C. Jarrell N. Cadotte F. St Michael E. Aberg C. M. Szymanski Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni J. Biol. Chem. 2002 277 42530 42539 (Pubitemid 35285620)
25. M. Wacker D. Linton P. G. Hitchen M. Nita-Lazar S. M. Haslam S. J. North M. Panico H. R. Morris A. Dell B. W. Wren M. Aebi N-Linked Glycosylation in Campylobacter jejuni and its functional transfer into E. coli Science 2002 298 1790 1793 (Pubitemid 35404123)
26. B. N. Fry V. Korolik J. A. ten Brinke M. T. T. Pennings R. Zalm B. J. J. Teunis P. J. Coloe B. A. M. van der Zeijst The lipopolysaccharide biosynthesis locus of Campylobacter jejuni 81116 Microbiology 1998 144 2049 2061 (Pubitemid 28403017)
27. A. V. Karlyshev P. Everest D. Linton S. Cawthraw D. G. Newell B. W. Wren The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks Microbiology 2004 150 1957 1964 (Pubitemid 38923693)
28. D. Linton E. Allan A. V. Karlyshev A. D. Cronshaw B. W. Wren Identification of N-cetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni Mol. Microbiol. 2002 43 497 508 (Pubitemid 34146738)
29. Y. Konto-Ghiorghi E. Mairey A. Mallet G. Dumenil E. Caliot P. Trieu-Cuot S. Dramsi Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae PLoS Pathog. 2009 5 e1000422
30. A. G. Manetti C. Zingaretti F. Falugi et al. (14 co-authors), Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation Mol. Microbiol. 2007 64 968 983 (Pubitemid 46743959)
31. L. Balonova L. Hernychova Z. Bilkova Bioanalytical tools for the discovery of eukaryotic glycoproteins applied to the analysis of bacterial glycoproteins Expert Rev. Proteomics 2009 6 75 85
32. P. G. Hitchen A. Dell Bacterial glycoproteomics Microbiology 2006 152 1575 1580
33. H. Li M. d'Anjou Pharmacological significance of glycosylation in therapeutic proteins Curr. Opin. Biotechnol. 2009 20 678 684
34. M. Daugherty B. Polanuyer M. Farrell M. Scholle A. Lykidis V. de Crecy-Lagard A. Osterman Complete reconstitution of the human coenzyme A biosynthetic pathway via comparative genomics J. Biol. Chem. 2002 277 21431 21439 (Pubitemid 34952284)
35. D. A. Johnson S. G. Tetu K. Phillippy J. Chen Q. Ren I. T. Paulsen High-throughput phenotypic characterization of Pseudomonas aeruginosa membrane transport genes PLoS Genet. 2008 4 e1000211
36. J. R. Cole B. Chai R. J. Farris Q. Wang A. S. Kulam-Syed-Mohideen D. M. McGarrell A. M. Bandela E. Cardenas G. M. Garrity J. M. Tiedje The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data Nucleic Acids Res. 2007 35 D169 D172
37. J. Peplies R. Kottmann W. Ludwig F. O. Glockner A standard operating procedure for phylogenetic inference (SOPPI) using (rRNA) marker genes Syst. Appl. Microbiol. 2008 31 251 257
38. G. L. Lorca R. D. Barabote V. Zlotopolski C. Tran B. Winnen R. N. Hvorup A. J. Stonestrom E. Nguyen L.-W. Huang D. S. Kim M. H. Saier, Jr. Transport capabilities of eleven Gram-positive bacteria: comparative genomic analyses Biochim. Biophys. Acta, Biomembr. 2007 1768 1342 1366 (Pubitemid 46782697)
39. R. Knauer L. Lehle The oligosaccharyltransferase complex from yeast Biochim. Biophys. Acta, Gen. Subj. 1999 1426 259 273 (Pubitemid 29027943)
40. R. Zufferey R. Knauer P. Burda I. Stagljar S. te Heesen L. Lehle M. Aebi STT3, a highly conserved protein required for yeast oligosaccharyltransferase activity in vivo EMBO J. 1995 14 4949 4960
41. M. F. Feldman M. Wacker M. Hernandez P. G. Hitchen C. L. Marolda M. Kowarik H. R. Morris A. Dell M. A. Valvano M. Aebi Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 2005 102 3016 3021 (Pubitemid 40299908)
42. M. Igura N. Maita J. Kamishikiryo M. Yamada T. Obita K. Maenaka D. Kohda Structure-guided identification of a new catalytic motif of oligosaccharyltransferase EMBO J. 2008 27 234 243
43. N. Maita J. Nyirenda M. Igura J. Kamishikiryo D. Kohda Comparative structural biology of eubacterial and archaeal oligosaccharyltransferases J. Biol. Chem. 2010 285 4941 4950
44. L. Li R. Woodward Y. Ding X.-w. Liu W. Yi V. S. Bhatt M. Chen L.-w. Zhang P. G. Wang Overexpression and topology of bacterial oligosaccharyltransferase PglB Biochem. Biophys. Res. Commun. 2010 394 1069 1074
45. C. Alaimo I. Catrein L. Morf C. L. Marolda N. Callewaert M. A. Valvano M. F. Feldman M. Aebi Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides EMBO J. 2006 25 967 976 (Pubitemid 43372111)
46. P. Guerry C. M. Szymanski Campylobacter sugars sticking out Trends Microbiol. 2008 16 428 435
47. U. B. Sleytr P. Messner D. Pum M. Sara Crystalline bacterial cell surface layers (S Layers): from supramolecular cell structure to biomimetics and nanotechnology Angew. Chem., Int. Ed. 1999 38 1034 1054
48. F. St Michael C. M. Szymanski J. Li K. H. Chan N. H. Khieu S. Larocque W. W. Wakarchuk J.-R. Brisson M. A. Monteiro The structures of the lipooligosaccharide and capsule polysaccharide of Campylobacter jejuni genome sequenced strain NCTC 11168 Eur. J. Biochem. 2002 269 5119 5136 (Pubitemid 35345126)
49. J. Van Heijenoort Recent advances in the formation of the bacterial peptidoglycan monomer unit Nat. Prod. Rep. 2001 18 503 519 (Pubitemid 33016991)
50. J. Parkhill B. W. Wren K. Mungall et al. (20 co-authors), The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable tracts Nature 2000 403 665 668 (Pubitemid 30104008)
51. P. M. Power M. P. Jennings The genetics of glycosylation in Gram-negative bacteria FEMS Microbiol. Lett. 2003 218 211 222 (Pubitemid 36183499)
52. S. Bernatchez C. M. Szymanski N. Ishiyama J. Li H. C. Jarrell P. C. Lau A. M. Berghuis N. M. Young W. W. Wakarchuk A single bifunctional UDP-GlcNAc/Glc 4-epimerase supports the synthesis of three cell surface glycoconjugates in Campylobacter jejuni J. Biol. Chem. 2005 280 4792 4802 (Pubitemid 40288651)
53. C. M. Kahler L. E. Martin Y. L. Tzeng Y. K. Miller K. Sharkey D. S. Stephens J. K. Davies Polymorphisms in pilin glycosylation locus of Neisseria meningitidis expressing class II pili Infect. Immun. 2001 69 3597 3604 (Pubitemid 32493273)
54. S. M. Logan J. F. Kelly P. Thibault C. P. Ewing P. Guerry Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins Mol. Microbiol. 2002 46 587 597 (Pubitemid 35340966)
55. I. C. Schoenhofen D. J. McNally E. Vinogradov D. Whitfield N. M. Young S. Dick W. W. Wakarchuk J.-R. Brisson S. M. Logan Functional characterization of dehydratase/aminotransferase pairs from Helicobacter and Campylobacter: enzymes distinguishing the pseudaminic acid and bacillosamine biosynthetic pathways J. Biol. Chem. 2006 281 723 732
56. L. L. Burrows R. V. Urbanic J. S. Lam Functional conservation of the polysaccharide biosynthetic protein WbpM and its homologues in Pseudomonas aeruginosa and other medically significant bacteria Infect. Immun. 2000 68 931 936 (Pubitemid 30056556)
57. C. Creuzenet J. S. Lam Topological and functional characterization of WbpM, an inner membrane UDP-GlcNAc C6 dehydratase essential for lipopolysaccharide biosynthesis in Pseudomonas aeruginosa Mol. Microbiol. 2001 41 1295 1310 (Pubitemid 32939502)
58. H. Guo L. Li P. G. Wang Biochemical characterization of UDP-GlcNAc/Glc 4-epimerase from Escherichia coli O86:B7 Biochemistry 2006 45 13760 13768 (Pubitemid 44788745)
59. H. Guo W. Yi L. Li P. G. Wang Three UDP-hexose 4-epimerases with overlapping substrate specificity coexist in E. coli O86:B7 Biochem. Biophys. Res. Commun. 2007 356 604 609 (Pubitemid 46499007)
60. E. Jaspers J. Overmann Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies Appl. Environ. Microbiol. 2004 70 4831 4839 (Pubitemid 39095511)
61. A. H. Stouthamer Metabolic pathways in Paracoccus denitrificans and closely related bacteria in relation to the phylogeny of prokaryotes Antonie van Leeuwenhoek 1991 61 1 33
62. S. C. Rison S. A. Teichmann J. M. Thornton Homology, pathway distance and chromosomal localization of the small molecule metabolism enzymes in Escherichia coli J. Mol. Biol. 2002 318 911 932 (Pubitemid 34729379)
63. S. Maslova S. Krishna T. Y. Panga K. Sneppen Toolbox model of evolution of prokaryotic metabolic networks and their regulation Proc. Natl. Acad. Sci. U. S. A. 2009 106 9743 9748
64. H. Isambert R. R. Stein On the need for widespread horizontal gene transfers under genome size constraint Biol. Direct 2009 4 28
65. E. V. Koonin Y. I. Wolf Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world Nucleic Acids Res. 2008 36 6688 6719
66. L. Aravind R. L. Tatusov Y. I. Wolf D. R. Walker E. V. Koonin Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles Trends Genet. 1998 14 442 444 (Pubitemid 28508919)
67. J. P. Gogarten W. F. Doolittle J. G. Lawrence Prokaryotic evolution in light of gene transfer Mol. Biol. Evol. 2002 19 2226 2238 (Pubitemid 35440456)
68. C. L. Nesbo S. L'Haridon K. O. Stetter W. F. Doolittle Phylogenetic analyses of two "archaeal" genes in Thermotoga maritima reveal multiple transfers between archaea and bacteria Mol. Biol. Evol. 2001 18 362 375 (Pubitemid 32225085)
69. T. Dagan W. Martin The tree of one percent Genome Biology 2006 7 118
70. P. T. Chippindale R. M. Bonett A. S. Baldwin J. J. Wiens Phylogenetic evidence for a major reversal of life-history evolution in plethodontid salamanders Evolution 2004 58 2809 2822 (Pubitemid 40084150)
71. R. Collin R. Cipriani Dollo's Law and the re-evolution of shell coiling Proc. R. Soc. London, Ser. B 2003 270 2551 2555 (Pubitemid 38082941)
72. R. Collin M. P. Miglietta Reversing opinions on Dollo's Law Trends Ecol. Evol. 2008 23 602 609
73. S. Light P. Kraulis Network analysis of metabolic enzyme evolution in Escherichia coli BMC Bioinformatics 2004 5 15
74. H. Ogata W. Fujibuchi S. Goto M. Kanehisa A heuristic graph comparison algorithm and its application to detect functionally related enzyme clusters Nucleic Acids Res. 2000 28 4021 4028
75. B. Snel P. Bork M. A. Huynen The identification of functional modules from the genomic association of genes Proc. Natl. Acad. Sci. U. S. A. 2002 99 5890 5895 (Pubitemid 34493235)
76. C. Von Mering E. M. Zdobnov S. Tsoka F. D. Ciccarelli J. B. Pereira-Leal C. A. Ouzounis P. Bork Genome evolution reveals biochemical networks and functional modules Proc. Natl. Acad. Sci. U. S. A. 2003 100 15428 15433 (Pubitemid 38021006)
77. T. Dandekar B. Snel M. Huynen P. Bork Conservation of gene order: a fingerprint of proteins that physically interact Trends Biochem. Sci. 1998 23 324 328 (Pubitemid 28461862)
78. G. V. Glazko A. R. Mushegian Detection of evolutionarily stable fragments of cellular pathways by hierarchical clustering of phyletic patterns Genome Biology 2004 5 R32
79. T. Itoh K. Takemoto H. Mori T. Gojobori Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes Mol. Biol. Evol. 1999 16 332 346 (Pubitemid 29119970)
80. E. V. Koonin A. R. Mushegian K. E. Rudd Sequencing and analysis of bacterial genomes Curr. Biol. 1996 6 404 416 (Pubitemid 126656288)
81. A. R. Mushegian E. V. Koonin Gene order is not conserved in bacterial evolution Trends Genet. 1996 12 289 290
82. J. Castresana Comparative genomics and bioenergetics Biochim. Biophys. Acta, Bioenerg. 2001 1506 147 162 (Pubitemid 34075225)
83. E. V. Koonin A. R. Mushegian P. Bork Non-orthologous gene displacement Trends Genet. 1996 12 334 336
84. D. R. Edgell W. F. Doolittle Archaea and the origin(s) of DNA replication proteins Cell 1997 89 995 998 (Pubitemid 127678731)
85. D. D. Leipe L. Aravind E. V. Koonin Did DNA replication evolve twice independently? Nucleic Acids Res. 1999 27 3389 3401 (Pubitemid 29414663)
86. S. F. Altschul W. Gish W. Miller E. W. Myers D. J. Lipman Basic local alignment search tool J. Mol. Biol. 1990 215 403 410
87. W. Gish D. J. States Identification of protein coding regions by database similarity search Nat. Genet. 1993 3 266 272 (Pubitemid 23096565)
88. P. Rice I. Longden A. Bleasby EMBOSS: The European Molecular Biology Open Software Suite Trends Genet. 2000 16 276 277
89. S. R. Eddy Profile hidden Markov models Bioinformatics 1998 14 755 763 (Pubitemid 28552108)
90. C. Notredame D. G. Higgins J. Heringa T-Coffee: a novel method for multiple sequence alignments J. Mol. Biol. 2000 302 205 217
91. A. Krogh B. Larsson G. von Heijne E. L. Sonnhammer Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol. 2001 305 567 580 (Pubitemid 33032862)
92. T. A. Hall BioEdit: a user-friendly biological sequence alignment eidtor and analysis program for Windows 95/98/NT Nucl. Acids Symp. Ser. 1999 41 95 98
93. K. Tamura J. Dudley M. Nei S. Kumar MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version4.0 Mol. Biol. Evol. 2007 24 1596 1599 (Pubitemid 47236692)
94. A. Marchler-Bauer J. B. Anderson F. Chitsaz et al. (27 co-authors), CDD: specific functional annotation with the Conserved Domain Database Nucleic Acids Res. 2009 37 D205 D210
95. R. D. Finn J. Mistry J. Tate et al. (16 co-authors), The Pfam protein families database Nucleic Acids Res. 2010 38 D211 D222
96. A. Schneider C. Dessimoz G. H. Gonnet OMA Browser - exploring orthologous relations across 352 complete genomes Bioinformatics 2007 23 2180 2182 (Pubitemid 47394120)
97. G. M. Garrity J. M. Tiedje The Ribosomal Database Project: improved alignments and new tools for rRNA analysis Nucleic Acids Res. 2009 37 D141 D145