1887

Abstract

Sialic acids are nine-carbon amino sugars that are present on all mucous membranes and are often used by bacteria as nutrients. In pathogenic the genes for sialic acid catabolism (SAC) are known to be important for host colonization, yet the route for sialic acid uptake is not proven. contains a tripartite ATP-independent periplasmic (TRAP) transporter, SiaPQM (VC1777–VC1779), encoded by genes within the pathogenicity island-2 (VPI-2), which are adjacent to the SAC genes , and . We demonstrate a correlation of the occurrence of VPI-2 and the ability of to grow on the common sialic acid -acetylneuraminic acid (Neu5Ac), and that a N16961 mutant defective in , encoding the large membrane protein component of the TRAP transporter, SiaM, is unable to grow on Neu5Ac as the sole carbon source. Using the genome context and known structures of the SiaP protein component of the TRAP transporter, we define a subfamily of Neu5Ac-specific TRAP transporters, of which the genes are the only representatives in . A recent report has suggested that an entirely different TRAP transporter (VC1927–VC1929) is the Neu5Ac transporter in . Bioinformatics and genomic analysis suggest strongly that this is a C-dicarboxylate-specific TRAP transporter, and indeed disruption of results in a defect in growth on C-dicarboxylates but not Neu5Ac. Together these data demonstrate unequivocally that the -encoded TRAP transporter within VPI-2 is the sole sialic acid transporter in .

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2012-08-01
2024-04-19
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References

  1. Allen S., Zaleski A., Johnston J. W., Gibson B. W., Apicella M. A. ( 2005). Novel sialic acid transporter of Haemophilus influenzae . Infect Immun 73:5291–5300 [View Article][PubMed]
    [Google Scholar]
  2. Almagro-Moreno S., Boyd E. F. ( 2009a). Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 9:118 [View Article][PubMed]
    [Google Scholar]
  3. Almagro-Moreno S., Boyd E. F. ( 2009b). Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 77:3807–3816 [View Article][PubMed]
    [Google Scholar]
  4. Brigham C., Caughlan R., Gallegos R., Dallas M. B., Godoy V. G., Malamy M. H. ( 2009). Sialic acid (N-acetyl neuraminic acid) utilization by Bacteroides fragilis requires a novel N-acetyl mannosamine epimerase. J Bacteriol 191:3629–3638 [View Article][PubMed]
    [Google Scholar]
  5. Chang D. E., Smalley D. J., Tucker D. L., Leatham M. P., Norris W. E., Stevenson S. J., Anderson A. B., Grissom J. E., Laux D. C. & other authors ( 2004). Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 101:7427–7432 [View Article][PubMed]
    [Google Scholar]
  6. Davies S. J., Golby P., Omrani D., Broad S. A., Harrington V. L., Guest J. R., Kelly D. J., Andrews S. C. ( 1999). Inactivation and regulation of the aerobic C4-dicarboxylate transport (dctA) gene of Escherichia coli . J Bacteriol 181:5624–5635[PubMed]
    [Google Scholar]
  7. Fischer M., Zhang Q. Y., Hubbard R. E., Thomas G. H. ( 2010). Caught in a TRAP: substrate-binding proteins in secondary transport. Trends Microbiol 18:471–478 [View Article][PubMed]
    [Google Scholar]
  8. Forward J. A., Behrendt M. C., Wyborn N. R., Cross R., Kelly D. J. ( 1997). TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse Gram-negative bacteria. J Bacteriol 179:5482–5493[PubMed]
    [Google Scholar]
  9. Galen J. E., Ketley J. M., Fasano A., Richardson S. H., Wasserman S. S., Kaper J. B. ( 1992). Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect Immun 60:406–415[PubMed]
    [Google Scholar]
  10. Golby P., Davies S., Kelly D. J., Guest J. R., Andrews S. C. ( 1999). Identification and characterization of a two-component sensor-kinase and response-regulator system (DcuS-DcuR) controlling gene expression in response to C4-dicarboxylates in Escherichia coli . J Bacteriol 181:1238–1248[PubMed]
    [Google Scholar]
  11. Hamblin M. J., Shaw J. G., Kelly D. J. ( 1993). Sequence analysis and interposon mutagenesis of a sensor-kinase (DctS) and response-regulator (DctR) controlling synthesis of the high-affinity C4-dicarboxylate transport system in Rhodobacter capsulatus . Mol Gen Genet 237:215–224 [View Article][PubMed]
    [Google Scholar]
  12. Heidelberg J. F., Eisen J. A., Nelson W. C., Clayton R. A., Gwinn M. L., Dodson R. J., Haft D. H., Hickey E. K., Peterson J. D. & other authors ( 2000). DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae . Nature 406:477–483 [View Article][PubMed]
    [Google Scholar]
  13. Horton R. M., Hunt H. D., Ho S. N., Pullen J. K., Pease L. R. ( 1989). Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61–68 [View Article][PubMed]
    [Google Scholar]
  14. Jeanmougin F., Thompson J. D., Gouy M., Higgins D. G., Gibson T. J. ( 1998). Multiple sequence alignment with clustal x . Trends Biochem Sci 23:403–405 [View Article][PubMed]
    [Google Scholar]
  15. Jeong H. G., Oh M. H., Kim B. S., Lee M. Y., Han H. J., Choi S. H. ( 2009). The capability of catabolic utilization of N-acetylneuraminic acid, a sialic acid, is essential for Vibrio vulnificus pathogenesis. Infect Immun 77:3209–3217 [View Article][PubMed]
    [Google Scholar]
  16. Jermyn W. S., Boyd E. F. ( 2002). Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 148:3681–3693[PubMed]
    [Google Scholar]
  17. Jermyn W. S., Boyd E. F. ( 2005). Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates. Microbiology 151:311–322 [View Article][PubMed]
    [Google Scholar]
  18. Johnston J. W., Coussens N. P., Allen S., Houtman J. C., Turner K. H., Zaleski A., Ramaswamy S., Gibson B. W., Apicella M. A. ( 2008). Characterization of the N-acetyl-5-neuraminic acid-binding site of the extracytoplasmic solute receptor (SiaP) of nontypeable Haemophilus influenzae strain 2019. J Biol Chem 283:855–865 [View Article][PubMed]
    [Google Scholar]
  19. Karaolis D. K., Johnson J. A., Bailey C. C., Boedeker E. C., Kaper J. B., Reeves P. R. ( 1998). A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci U S A 95:3134–3139 [View Article][PubMed]
    [Google Scholar]
  20. Kim Y. R., Lee S. E., Kim C. M., Kim S. Y., Shin E. K., Shin D. H., Chung S. S., Choy H. E., Progulske-Fox A. & other authors ( 2003). Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect Immun 71:5461–5471 [View Article][PubMed]
    [Google Scholar]
  21. Kleefeld A., Ackermann B., Bauer J., Krämer J., Unden G. ( 2009). The fumarate/succinate antiporter DcuB of Escherichia coli is a bifunctional protein with sites for regulation of DcuS-dependent gene expression. J Biol Chem 284:265–275 [View Article][PubMed]
    [Google Scholar]
  22. Kovach M. E., Shaffer M. D., Peterson K. M. ( 1996). A putative integrase gene defines the distal end of a large cluster of ToxR-regulated colonization genes in Vibrio cholerae . Microbiology 142:2165–2174 [View Article][PubMed]
    [Google Scholar]
  23. Lubin J. B., Kingston J. J., Chowdhury N., Boyd E. F. ( 2012). Sialic acid catabolism and transport gene clusters are lineage specific in Vibrio vulnificus . Appl Environ Microbiol 78:3407–3415 [View Article][PubMed]
    [Google Scholar]
  24. Makino K., Oshima K., Kurokawa K., Yokoyama K., Uda T., Tagomori K., Iijima Y., Najima M., Nakano M. & other authors ( 2003). Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae . Lancet 361:743–749 [View Article][PubMed]
    [Google Scholar]
  25. Müller A., Severi E., Mulligan C., Watts A. G., Kelly D. J., Wilson K. S., Wilkinson A. J., Thomas G. H. ( 2006). Conservation of structure and mechanism in primary and secondary transporters exemplified by SiaP, a sialic acid binding virulence factor from Haemophilus influenzae . J Biol Chem 281:22212–22222 [View Article][PubMed]
    [Google Scholar]
  26. Mulligan C., Geertsma E. R., Severi E., Kelly D. J., Poolman B., Thomas G. H. ( 2009). The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter. Proc Natl Acad Sci U S A 106:1778–1783 [View Article][PubMed]
    [Google Scholar]
  27. Mulligan C., Fischer M., Thomas G. H. ( 2011). Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea. FEMS Microbiol Rev 35:68–86 [View Article][PubMed]
    [Google Scholar]
  28. Mulligan C., Leech A. P., Kelly D. J., Thomas G. H. ( 2012). The membrane proteins SiaQ and SiaM form an essential stoichiometric complex in the sialic acid tripartite ATP-independent periplasmic (TRAP) transporter SiaPQM (VC1777–1779) from Vibrio cholerae . J Biol Chem 287:3598–3608 [View Article][PubMed]
    [Google Scholar]
  29. Nees S., Schauer R., Mayer F., Ehrlich K. ( 1976). Purification and characterization of N-acetylneuraminate lyase from Clostridium perfringens . Hoppe Seylers Z Physiol Chem 357:839–853 [View Article][PubMed]
    [Google Scholar]
  30. Pearson M. D., Noller H. F. ( 2011). The draft genome of Planococcus donghaensis MPA1U2 reveals nonsporulation pathways controlled by a conserved Spo0A regulon. J Bacteriol 193:6106 [View Article][PubMed]
    [Google Scholar]
  31. Philippe N., Alcaraz J. P., Coursange E., Geiselmann J., Schneider D. ( 2004). Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51:246–255 [View Article][PubMed]
    [Google Scholar]
  32. Roy S., Douglas C. W., Stafford G. P. ( 2010). A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia . J Bacteriol 192:2285–2293 [View Article][PubMed]
    [Google Scholar]
  33. Saitou N., Nei M. ( 1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  34. Severi E., Randle G., Kivlin P., Whitfield K., Young R., Moxon R., Kelly D., Hood D., Thomas G. H. ( 2005). Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol Microbiol 58:1173–1185 [View Article][PubMed]
    [Google Scholar]
  35. Severi E., Hood D. W., Thomas G. H. ( 2007). Sialic acid utilization by bacterial pathogens. Microbiology 153:2817–2822 [View Article][PubMed]
    [Google Scholar]
  36. Severi E., Müller A., Potts J. R., Leech A., Williamson D., Wilson K. S., Thomas G. H. ( 2008). Sialic acid mutarotation is catalyzed by the Escherichia coli beta-propeller protein YjhT. J Biol Chem 283:4841–4849 [View Article][PubMed]
    [Google Scholar]
  37. Severi E., Hosie A. H., Hawkhead J. A., Thomas G. H. ( 2010). Characterization of a novel sialic acid transporter of the sodium solute symporter (SSS) family and in vivo comparison with known bacterial sialic acid transporters. FEMS Microbiol Lett 304:47–54 [View Article][PubMed]
    [Google Scholar]
  38. Sharma S. K., Moe T. S., Srivastava R., Chandra D., Srivastava B. S. ( 2011a). Functional characterization of VC1929 of Vibrio cholerae El Tor: role in mannose-sensitive haemagglutination, virulence and utilization of sialic acid. Microbiology 157:3180–3186 [View Article][PubMed]
    [Google Scholar]
  39. Sharma S. K., Moe T. S., Srivastava R., Chandra D., Srivastava B. S. ( 2011b). Authors’ response: on sialic acid transport and utilization by Vibrio cholerae . Microbiology 157:3254–3255 [View Article][PubMed]
    [Google Scholar]
  40. Shaw J. G., Hamblin M. J., Kelly D. J. ( 1991). Purification, characterization and nucleotide sequence of the periplasmic C4-dicarboxylate-binding protein (DctP) from Rhodobacter capsulatus . Mol Microbiol 5:3055–3062 [View Article][PubMed]
    [Google Scholar]
  41. Six S., Andrews S. C., Unden G., Guest J. R. ( 1994). Escherichia coli possesses two homologous anaerobic C4-dicarboxylate membrane transporters (DcuA and DcuB) distinct from the aerobic dicarboxylate transport system (Dct). J Bacteriol 176:6470–6478[PubMed]
    [Google Scholar]
  42. Steenbergen S. M., Lichtensteiger C. A., Caughlan R., Garfinkle J., Fuller T. E., Vimr E. R. ( 2005). Sialic acid metabolism and systemic pasteurellosis. Infect Immun 73:1284–1294 [View Article][PubMed]
    [Google Scholar]
  43. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. ( 2011). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  44. Taylor R. K., Miller V. L., Furlong D. B., Mekalanos J. J. ( 1987). Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci U S A 84:2833–2837 [View Article][PubMed]
    [Google Scholar]
  45. Thomas G. H., Boyd E. F. ( 2011). On sialic acid transport and utilization by Vibrio cholerae . Microbiology 157:3253–3254 [View Article][PubMed]
    [Google Scholar]
  46. Thomas G. H., Southworth T., León-Kempis M. R., Leech A., Kelly D. J. ( 2006). Novel ligands for the extracellular solute receptors of two bacterial TRAP transporters. Microbiology 152:187–198 [View Article][PubMed]
    [Google Scholar]
  47. Valentini M., Storelli N., Lapouge K. ( 2011). Identification of C4-dicarboxylate transport systems in Pseudomonas aeruginosa PAO1. J Bacteriol 193:4307–4316 [View Article][PubMed]
    [Google Scholar]
  48. Varki A. ( 1992). Diversity in the sialic acids. Glycobiology 2:25–40 [View Article][PubMed]
    [Google Scholar]
  49. Varki A. ( 2008). Sialic acids in human health and disease. Trends Mol Med 14:351–360 [View Article][PubMed]
    [Google Scholar]
  50. Vimr E., Lichtensteiger C. ( 2002). To sialylate, or not to sialylate: that is the question. Trends Microbiol 10:254–257 [View Article][PubMed]
    [Google Scholar]
  51. Vimr E. R., Troy F. A. ( 1985). Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli . J Bacteriol 164:845–853[PubMed]
    [Google Scholar]
  52. Vimr E. R., Kalivoda K. A., Deszo E. L., Steenbergen S. M. ( 2004). Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68:132–153 [View Article][PubMed]
    [Google Scholar]
  53. Waldor M. K., Mekalanos J. J. ( 1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914 [View Article][PubMed]
    [Google Scholar]
  54. Zientz E., Six S., Unden G. ( 1996). Identification of a third secondary carrier (DcuC) for anaerobic C4-dicarboxylate transport in Escherichia coli: roles of the three Dcu carriers in uptake and exchange. J Bacteriol 178:7241–7247[PubMed]
    [Google Scholar]
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