Genomic and metabolic profiling of nonulosonic acids in Vibrionaceae reveal biochemical phenotypes of allelic divergence in Vibrio vulnificus

Applied and Environmental Microbiology

Volumn 77, Issue 16, 2011, Pages 5782-5793

  Lewis, Amanda L ^a   Lubin, Jean Bernard ^c   Argade, Shilpa ^b   Naidu, Natasha ^b   Choudhury, Biswa ^b   Boyd, E Fidelma ^c  

^a WASHINGTON UNIVERSITY   (United States)

^b University of California San Diego   (United States)

^c UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ANALYSIS; BIOCHEMICAL PHENOTYPES; BIOSYNTHESIS PATHWAYS; CELL SURFACES; CLINICAL ISOLATES; ENVIRONMENTAL ISOLATES; GENE CLUSTERS; GLYCOCONJUGATES; HORIZONTAL TRANSFER; HOT SPOT; HUMAN PATHOGENS; LARGE GROUPS; METABOLIC PROFILING; SIALIC ACIDS; TERMINAL POSITION; VIBRIO VULNIFICUS; VIBRIONACEAE;

BACTERIA; BIOCHEMISTRY; CARBOXYLIC ACIDS; CELL MEMBRANES; DNA SEQUENCES; MAMMALS; MASS SPECTROMETRY; SUGARS;

GENES;

BACTERIAL DNA; N ACETYLNEURAMINIC ACID;

ALLELE; BACTERIUM; BIOCHEMICAL COMPOSITION; CARBON; CLUSTER ANALYSIS; DIVERGENCE; GENETIC ANALYSIS; GENOMICS; MAMMAL; MASS SPECTROMETRY; METABOLISM; MOLECULAR ANALYSIS; NUMERICAL MODEL; ORGANIC ACID; PHENOTYPE; PHYLOGENETICS; RECOMBINATION; SPECIALIZATION; SPECIES DIVERSITY;

ALLELE; ARTICLE; BACTERIAL GENOME; BACTERIUM IDENTIFICATION; BIOLOGY; BIOSYNTHESIS; GENETIC VARIABILITY; GENETICS; METABOLISM; METABOLOME; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; RNA GENE; VIBRIONACEAE;

ALLELES; BACTERIAL TYPING TECHNIQUES; BASE SEQUENCE; BIOSYNTHETIC PATHWAYS; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; GENES, RRNA; GENETIC VARIATION; GENOME, BACTERIAL; METABOLOME; MULTIGENE FAMILY; N-ACETYLNEURAMINIC ACID; PHENOTYPE; PHYLOGENY; VIBRIONACEAE;

ANIMALIA; MAMMALIA; VIBRIO VULNIFICUS; VIBRIONACEAE;

EID: 80052619793     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00712-11     Document Type: Article

References (64)

1. Anderson, G. G., C. C. Goller, S. Justice, S. J. Hultgren, and P. C. Seed. 2010. Polysaccharide capsule and sialic acid-mediated regulation promote biofilm-like intracellular bacterial communities during cystitis. Infect. Immun. 78:963-975.
2. Angata, T., and A. Varki. 2002. Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem. Rev. 102:439-469.
3. Austin, B. 2010. Vibrios as causal agents of zoonoses. Vet. Microbiol. 140: 310-317.
4. Bisharat, N., C. Amaro, B. Fouz, A. Llorens, and D. I. Cohen. 2007. Serological and molecular characteristics of Vibrio vulnificus biotype 3: evidence for high clonality. Microbiology 153:847-856.
5. Bisharat, N., et al. 2005. Hybrid Vibrio vulnificus. Emerg. Infect. Dis. 11:30-35.
6. Bisharat, N., et al. 2007. The evolution of genetic structure in the marine pathogen, Vibrio vulnificus. Infect. Genet. Evol. 7:685-693.
7. Bøgwald, J., and J. Hoffman. 2006. Structural studies of the O-antigenic oligosaccharide from Vibrio salmonicida strain C2 isolated from Atlantic cod, Gadus morhua L. Carbohydr. Res. 341:1965-1968.
8. Carlin, A. F., A. L. Lewis, A. Varki, and V. Nizet. 2007. Group B streptococcal capsular sialic acids interact with siglecs (immunoglobulin-like lectins) on human leukocytes. J. Bacteriol. 189:1231-1237.
9. Carlin, A. F., et al. 2009. Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response. Blood 113:3333-3336.
10. Chen, C. Y., et al. 2003. Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res. 13:2577-2587.
11. Cohen, A. L., J. D. Oliver, A. DePaola, E. J. Feil, and E. F. Boyd. 2007. Emergence of a virulent clade of Vibrio vulnificus and correlation with the presence of a 33-kilobase genomic island. Appl. Environ. Microbiol. 73: 5553-5565.
12. DePaola, A., G. M. Capers, and D. Alexander. 1994. Densities of Vibrio vulnificus in the intestines of fish from the U.S. Gulf Coast. Appl. Environ. Microbiol. 60:984-988.
13. Edebrink, P., P. E. Jansson, J. Bøgwald, and J. Hoffman. 1996. Structural studies of the Vibrio salmonicida lipopolysaccharide. Carbohydr. Res. 287: 225-245.
14. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
15. Ewing, C. P., E. Andreishcheva, and P. Guerry. 2009. Functional characterization of flagellin glycosylation in Campylobacter jejuni 81-176. J. Bacteriol. 191:7086-7093.
16. Gil-Serrano, A. M., et al. 1999. Structural determination of a 5-acetamido-3,5,7,9-tetradeoxy-7-(3-hydroxybutyramido)-L-glycero-L-manno-nonulosonic acid-containing homopolysaccharide isolated from Sinorhizobium fredii HH103. Biochem. J. 342(Pt. 3):527-535.
17. Grimes, D. J., et al. 2009. What genomic sequence information has revealed about Vibrio ecology in the ocean-a review. Microb. Ecol. 58:447-460.
18. Guerry, P., et al. 2006. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 60:299-311.
19. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
20. Guindon, S., F. Lethiec, P. Duroux, and O. Gascuel. 2005. PHYML Online- a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33:W557-W559.
21. Heidelberg, J. F., K. B. Heidelberg, and R. R. Colwell. 2002. Bacteria of the gamma-subclass Proteobacteria associated with zooplankton in Chesapeake Bay. Appl. Environ. Microbiol. 68:5498-5507.
22. Heidelberg, J. F., K. B. Heidelberg, and R. R. Colwell. 2002. Seasonality of Chesapeake Bay bacterioplankton species. Appl. Environ. Microbiol. 68: 5488-5497.
23. Higa, H. H., C. Butor, S. Diaz, and A. Varki. 1989. O-acetylation and de-O-acetylation of sialic acids. O-acetylation of sialic acids in the rat liver Golgi apparatus involves an acetyl intermediate and essential histidine and lysine residues-a transmembrane reaction? J. Biol. Chem. 264:19427-19434.
24. Houliston, R. S., et al. 2011. The lipooligosaccharide of Campylobacter jejuni: similarity with multiple types of mammalian glycans beyond gangliosides. J. Biol. Chem. 286:12361-12370.
25. Huson, D. H. 1998. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68-73.
26. Jones, C., M. Virji, and P. R. Crocker. 2003. Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol. Microbiol. 49:1213-1225.
27. Jones, M. K., and J. D. Oliver. 2009. Vibrio vulnificus: disease and pathogenesis. Infect. Immun. 77:1723-1733.
28. Kaysner, C. A., et al. 1987. Virulent strains of Vibrio vulnificus isolated from estuaries of the United States West Coast. Appl. Environ. Microbiol. 53: 1349-1351.
29. Kaysner, C. A., M. L. Tamplin, M. M. Wekell, R. F. Stott, and K. G. Colburn. 1989. Survival of Vibrio vulnificus in shellstock and shucked oysters (Crassostrea gigas and Crassostrea virginica) and effects of isolation medium on recovery. Appl. Environ. Microbiol. 55:3072-3079.
30. Khatua, B., et al. 2010. Sialic acids acquired by Pseudomonas aeruginosa are involved in reduced complement deposition and siglec mediated host-cell recognition. FEBS Lett. 584:555-561.
31. Knirel, Y. A., A. S. Shashkov, Y. E. Tsvetkov, P. E. Jansson, and U. Zahringer. 2003. 5,7-Diamino-3,5,7,9-tetradeoxynon-2-ulosonic acids in bacterial glycopolymers: chemistry and biochemistry. Adv. Carbohydr. Chem. Biochem. 58:371-417.
32. Komagamine, T., and N. Yuki. 2006. Ganglioside mimicry as a cause of Guillain-Barré syndrome. CNS Neurol. Disord. Drug Targets 5:391-400.
33. Larkin, M. A., et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
34. Le Quéré, A. J., et al. 2006. Structural characterization of a K-antigen capsular polysaccharide essential for normal symbiotic infection in Rhizobium sp. NGR234: deletion of the rkpMNO locus prevents synthesis of 5,7-diacetamido-3,5,7,9-tetradeoxy-non-2-ulosonic acid. J. Biol. Chem. 281: 28981-28992.
35. Lewis, A. L., et al. 2009. Innovations in host and microbial sialic acid biosynthesis revealed by phylogenomic prediction of nonulosonic acid structure. Proc. Natl. Acad. Sci. U. S. A. 106:13552-13557.
36. Lewis, A. L., V. Nizet, and A. Varki. 2004. Discovery and characterization of sialic acid O-acetylation in group B Streptococcus. Proc. Natl. Acad. Sci. U. S. A. 101:11123-11128.
37. Li, X., et al. 2010. Structural and genetic characterization of the O-antigen of Escherichia coli O161 containing a derivative of a higher acidic diamino sugar, legionaminic acid. Carbohydr. Res. 345:1581-1587.
38. Linkous, D. A., and J. D. Oliver. 1999. Pathogenesis of Vibrio vulnificus. FEMS Microbiol. Lett. 174:207-214.
39. Linton, D., et al. 2000. Multiple N-acetyl neuraminic acid synthetase (neuB) genes in Campylobacter jejuni: identification and characterization of the gene involved in sialylation of lipo-oligosaccharide. Mol. Microbiol. 35:1120-1134.
40. Logan, S. M., et al. 2009. Identification of novel carbohydrate modifications on Campylobacter jejuni 11168 flagellin using metabolomics-based approaches. FEBS J. 276:1014-1023.
41. Logan, S. M., J. F. Kelly, P. Thibault, C. P. Ewing, and P. Guerry. 2002. Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins. Mol. Microbiol. 46:587-597.
42. McNally, D. J., et al. 2007. Targeted metabolomics analysis of Campylobacter coli VC167 reveals legionaminic acid derivatives as novel flagellar glycans. J. Biol. Chem. 282:14463-14475.
43. McNally, D. J., et al. 2006. Functional characterization of the flagellar glycosylation locus in Campylobacter jejuni 81-176 using a focused metabolomics approach. J. Biol. Chem. 281:18489-18498.
44. Motes, M. L., et al. 1998. Influence of water temperature and salinity on Vibrio vulnificus in Northern Gulf and Atlantic Coast oysters (Crassostrea virginica). Appl. Environ. Microbiol. 64:1459-1465.
45. Naito, M., et al. 2010. Effects of sequential Campylobacter jejuni 81-176 lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J. Bacteriol. 192:2182-2192.
46. Oliver, J. D. 1995. The viable but non-culturable state in the human pathogen Vibrio vulnificus. FEMS Microbiol. Lett. 133:203-208.
47. Oliver, J. D. 2005. Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiol. Infect. 133:383-391.
48. Perepelov, A. V., et al. 2010. Structure of the O-antigen and characterization of the O-antigen gene cluster of Escherichia coli O108 containing 5,7-diacetamido-3,5,7,9-tetradeoxy-L-glycero-D-galacto-non-2-ulosonic (8-epilegionaminic) acid. Biochemistry (Mosc.) 75:19-24.
49. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
50. Schirm, M., et al. 2003. Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori. Mol. Microbiol. 48:1579-1592.
51. Shashkov, A. S., et al. 2007. Structure of the O-antigen of Providencia stuartii O20, a new polysaccharide containing 5,7-diacetamido-3,5,7,9-tetradeoxy-Lglycero-D-galacto-non-2-ulosonic acid. Carbohydr. Res. 342:653-658.
52. Swords, W. E., et al. 2004. Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infect. Immun. 72:106-113.
53. Tamplin, M., G. E. Rodrick, N. J. Blake, and T. Cuba. 1982. Isolation and characterization of Vibrio vulnificus from two Florida estuaries. Appl. Environ. Microbiol. 44:1466-1470.
54. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
55. Varki, A. 2007. Glycan-based interactions involving vertebrate sialic-acidrecognizing proteins. Nature 446:1023-1029.
56. Vimr, E., and C. Lichtensteiger. 2002. To sialylate, or not to sialylate: that is the question. Trends Microbiol. 10:254-257.
57. Vimr, E. R., K. A. Kalivoda, E. L. Deszo, and S. M. Steenbergen. 2004. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68:132-153.
58. Vinogradov, E., et al. 2009. Structure of the lipopolysaccharide core of Vibrio vulnificus type strain 27562. Carbohydr. Res. 344:484-490.
59. Warner, E. B., and J. D. Oliver. 2008. Multiplex PCR assay for detection and simultaneous differentiation of genotypes of Vibrio vulnificus biotype 1. Foodborne Pathog. Dis. 5:691-693.
60. Warner, J. M., and J. D. Oliver. 1999. Randomly amplified polymorphic DNA analysis of clinical and environmental isolates of Vibrio vulnificus and other vibrio species. Appl. Environ. Microbiol. 65:1141-1144.
61. Warren, L. 1963. The distribution of sialic acids in nature. Comp. Biochem. Physiol. 10:153-171.
62. Warren, L. 1959. The thiobarbituric acid assay of sialic acids. J. Biol. Chem. 234:1971-1975.
63. Wessels, M. R., C. E. Rubens, V. J. Benedi, and D. L. Kasper. 1989. Definition of a bacterial virulence factor: sialylation of the group B streptococcal capsule. Proc. Natl. Acad. Sci. U. S. A. 86:8983-8987.
64. Wu, H., and A. E. Jerse. 2006. Alpha-2,3-sialyltransferase enhances Neisseria gonorrhoeae survival during experimental murine genital tract infection. Infect. Immun. 74:4094-4103.