Identification of a putative glycosyltransferase responsible for the transfer of pseudaminic acid onto the polar flagellin of Aeromonas caviae Sch3N

MicrobiologyOpen

Volumn 1, Issue 2, 2012, Pages 149-160

  Parker, Jennifer L ^a   Day Williams, Michaela J ^a   Tomas, Juan M ^b   Stafford, Graham P ^c   Shaw, Jonathan G ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Aeromonas; Flagella; Motility

Indexed keywords

2 OXOACID; FLAGELLIN; GLYCAN DERIVATIVE; GLYCOSYLTRANSFERASE; LIPOPOLYSACCHARIDE; PROTEIN FLAA; PROTEIN FLAB; PSEUDAMINIC ACID; SERINE; THREONINE; UNCLASSIFIED DRUG;

AEROMONAS PUNCTATA; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIUM MOTILITY; BACTERIUM MUTANT; BIOINFORMATICS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ANALYSIS; FLAA GENE; GENE LOCUS; GENETIC TRANSCRIPTION; GLYCOSYLATION; IMMUNOBLOTTING; MAF1 GENE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE;

EID: 84879499648     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.19     Document Type: Article

References (33)

1. Canals, R., S. Vilches, M. Wilhelms, J. G. Shaw, Merino, S. andJ. M. Tomas. 2007. Non-structural flagella genes affecting both polar and lateral flagella-mediated motility in Aeromonas hydrophila. Microbiology 153:1165-1175.
2. Chiu, C. P., A. G. Watts, L. L. Lairson, M. Gilbert, D. Lim, W. W. Wakarchuk, S. G. Withers, and N. C. Strynadka. 2004. Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog. Nat. Struct. Mol. Biol. 11:163-170.
3. De Lorenzo, V., M. Herrero, U. Jakubzik, and K. N. Timmis. 1990. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J. Bacteriol. 172:6568-6572.
4. Erhardt, M., K. Namba, and K. T. Hughes. 2010. Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb. Perspect. Biol. 2:a000299.
5. Fletcher, C. M., M. J. Coyne, and L. E. Comstock. 2011. Theoretical and experimental characterization of the scope of protein O-glycosylation in Bacteroides fragilis. J. Biol. Chem. 286:3219-3226.
6. Gavin, R., A. A. Rabaan, S. Merino, J. M. Tomas, I. Gryllos, and J. G. Shaw. 2002. Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43:383-397.
7. Goon, S., J. F. Kelly, S. M. Logan, C. P. Ewing, and P. Guerry. 2003. Pseudaminic acid, the major modification on Campylobacter flagellin, is synthesized via the Cj1293 gene. Mol. Microbiol. 50:659-671.
8. Gryllos, I., J. G. Shaw, R. Gavin, S. Merino, and J. M. Tomas. 2001. Role of flm locus in mesophilic Aeromonas species adherence. Infect. Immun. 69:65-74.
9. Guard-Petter, J., B. Lakshmi, R. Carlson, and K. Ingram. 1995. Characterization of lipopolysaccharide heterogeneity in Salmonella enteritidis by an improved gel electrophoresis method. Appl. Environ. Microbiol. 61:2845-2851.
10. Herrero, M., V. De Lorenzo & K. N. Timmis 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172:6557-6567.
11. Hirano, T., T. Minamino, K. Namba, and R. M. Macnab. 2003. Substrate specificity classes and the recognition signal for Salmonella type III flagellar export. J. Bacteriol. 185:2485-2492.
12. Imai, K., N. Asakawa, T. Tsuji, F. Akazawa, A. Ino, M. Sonoyama, and S. Mitaku. 2008. SOSUI-GramN: high performance prediction for sub-cellular localization of proteins in gram-negative bacteria. Bioinformation 2:417-421.
13. Janda, J. M., and S. L. Abbott. 2010. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev. 23:35-73.
14. Josenhans, C., L. Vossebein, S. Friedrich, and S. Suerbaum. 2002. The neuA/flmD gene cluster of Helicobacter pylori is involved in flagellar biosynthesis and flagellin glycosylation. FEMS Microbiol. Lett. 210:165-172.
15. Kaniga, K., I. Delor, and G. R. Cornelis. 1991. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137-141.
16. Karlyshev, A. V., D. Linton, N. A. Gregson, and B. W. Wren. 2002. A novel paralogous gene family involved in phase-variable flagella-mediated motility in Campylobacter jejuni. Microbiology 148:473-480.
17. Kirov, S. M., B. C. Tassell, A. B. Semmler, L. A. O'Donovan, A. A. Rabaan, and J. G. Shaw. 2002. Lateral flagella and swarming motility in Aeromonas species. J. Bacteriol. 184:547-555.
18. Kovach, M. E., R. W. Phillips, P. H. Elzer, R. M. Roop, 2nd, and K. M. Peterson. 1994. pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16:800-802.
19. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop, 2nd, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
20. Leclerc, G., S. P. Wang, and B. Ely. 1998. A new class of Caulobacter crescentus flagellar genes. J. Bacteriol. 180:5010-5019.
21. Logan, S. M. 2006. Flagellar glycosylation-a new component of the motility repertoire? Microbiology 152:1249-1262.
22. Marchler-Bauer, A., S. Lu, J. B. Anderson, F. Chitsaz, M. K. Derbyshire, C. Deweese-Scott, J. H. Fong, L. Y. Geer, R. C. Geer, N. R. Gonzales, et al. 2011. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 39:D225-D229.
23. McNally, D. J., J. P. Hui, A. J. Aubry, K. K. Mui, P. Guerry, J. R. Brisson, S. M. Logan, and E. C. Soo. 2006. Functional characterization of the flagellar glycosylation locus in Campylobacter jejuni 81-176 using a focused metabolomics approach. J. Biol. Chem. 281:18489-18498.
24. Nogueras, M. M., S. Merino, A. Aguilar, V. J. Benedi, and J. M. Tomas. 2000. Cloning, sequencing, and role in serum susceptibility of porin II from mesophilic Aeromonas hydrophila. Infect. Immun. 68:1849-1854.
25. Nothaft, H., and C. M. Szymanski. 2010. Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8:765-778.
26. Parker, J. L., and J. G. Shaw. 2011. Aeromonas spp. clinical microbiology and disease. J. Infect. 62:109-118.
27. Rabaan, A. A., I. Gryllos, J. M. Tomas, and J. G. Shaw. 2001. Motility and the polar flagellum are required for Aeromonas caviae adherence to HEp-2 cells. Infect. Immun. 69:4257-4267.
28. Schirm, M., E. C. Soo, A. J. Aubry, J. Austin, P. Thibault, and S. M. Logan. 2003. Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori. Mol. Microbiol. 48:1579-1592.
29. Schirm, M., S. K. Arora, A. Verma, E. Vinogradov, P. Thibault, R. Ramphal, and S. M. Logan. 2004. Structural and genetic characterization of glycosylation of type a flagellin in Pseudomonas aeruginosa. J. Bacteriol. 186:2523-2531.
30. Schoenhofen, I. C., D. J. McNally, J. R. Brisson, and S. M. Logan. 2006. Elucidation of the CMP-pseudaminic acid pathway in Helicobacter pylori: synthesis from UDP-N-acetylglucosamine by a single enzymatic reaction. Glycobiology 16:8C-14C.
31. Tabei, S. M., P. G. Hitchen, M. J. Day-Williams, S. Merino, R. Vart, P. C. Pang, G. J. Horsburgh, S. Viches, M. Wilhelms, J. M. Tomas, et al. 2009. An Aeromonas caviae genomic island is required for both O-antigen lipopolysaccharide biosynthesis and flagellin glycosylation. J. Bacteriol. 191:2851-2863.
32. Thibault, P., S. M. Logan, J. F. Kelly, J. R. Brisson, C. P. Ewing, T. J. Trust, and P. Guerry. 2001. Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem. 276:34862-34870.
33. Verma, A., M. Schirm, S. K. Arora, P. Thibault, S. M. Logan, and R. Ramphal. 2006. Glycosylation of b-Type flagellin of Pseudomonas aeruginosa: structural and genetic basis. J. Bacteriol. 188:4395-4403.