Multi-omics approaches to deciphering a hypervirulent strain of Campylobacter jejuni

Genome Biology and Evolution

Volumn 5, Issue 11, 2013, Pages 2217-2230

  Wu, Zuowei ^a   Sahin, Orhan ^a   Shen, Zhangqi ^a   Liu, Peng ^a   Miller, William G ^b   Zhang, Qijing ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b WESTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

Campylobacter jejuni; Comparative genomics; Functional genomics; Virulence evolution

Indexed keywords

BACTERIAL POLYSACCHARIDE; PROTEOME; TRANSCRIPTOME;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BIOSYNTHESIS; CAMPYLOBACTER JEJUNI; COMPARATIVE GENOMICS; FUNCTIONAL GENOMICS; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; METABOLISM; PATHOGENICITY; PLASMID; SINGLE NUCLEOTIDE POLYMORPHISM; SYNTENY; VIRULENCE; VIRULENCE EVOLUTION;

CAMPYLOBACTER JEJUNI; COMPARATIVE GENOMICS; FUNCTIONAL GENOMICS; VIRULENCE EVOLUTION;

CAMPYLOBACTER JEJUNI; CHROMOSOMES, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GLYCOSYLATION; PLASMIDS; POLYMORPHISM, SINGLE NUCLEOTIDE; POLYSACCHARIDES, BACTERIAL; PROTEOME; SYNTENY; TRANSCRIPTOME; VIRULENCE;

EID: 84892658325     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt172     Document Type: Article

References (82)

1. Adak GK, Meakins SM, Yip H, Lopman BA, O'Brien SJ. 2005. Disease risks from foods, England and Wales, 1996-2000. Emerg Infect Dis. 11:365-372.
2. Bacon DJ, et al. 2000. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun. 68:4384-4390.
3. Bacon DJ, et al. 2002. DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81-176. Infect Immun. 70:6242-6250.
4. Banerjee HN, et al. 2012. Search for a diagnostic/prognostic biomarker for the brain cancer glioblastoma multiforme by 2D-DIGE-MS technique. Mol Cell Biochem. 367:59-63.
5. Brinig MM, et al. 2006. Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J Bacteriol. 188:2375-2382.
6. Brown JR, Douady CJ, Italia MJ, Marshall WE, Stanhope MJ. 2001. Universal trees based on large combined protein sequence data sets. Nat Genet. 28:281-285.
7. Burrough ER, Sahin O, Plummer PJ, Zhang Q, Yaeger MJ. 2009. Pathogenicity of an emergent, ovine abortifacient Campylobacter jejuni clone orally inoculated into pregnant guinea pigs. Am J Vet Res. 70:1269-1276.
8. Camacho C, et al. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421.
9. Carrillo CD, et al. 2004. Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J Biol Chem. 279:20327-20338.
10. Dari L, Rabinowitz JC. 1991. Purification, characterization, cloning, and amino-acid-sequence of the bifunctional enzyme 5, 10-methylenetetrahydrofolate dehydrogenase/5, 10-methenyltetrahydrofolate cyclohydrolase from Escherichia coli. J Biol Chem. 266:23953-23958.
11. Davis LM, Kakuda T, DiRita VJ. 2009. A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J Bacteriol. 191:1631-1640.
12. Delong WJ, Jaworski MD, Ward AC. 1996. Antigenic and restriction enzyme analysis of Campylobacter spp associated with abortion in sheep. Am J Vet Res. 57:163-167.
13. Dorrell N, et al. 2001. Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. Genome Res. 11:1706-1715.
14. Elliott KT, Dirita VJ. 2008. Characterization of CetA and CetB, a bipartite energy taxis system in Campylobacter jejuni. Mol Microbiol. 69:1091-1103.
15. Elvers KT, et al. 2005. NssR, a member of the Crp-Fnr superfamily from Campylobacter jejuni, regulates a nitrosative stress-responsive regulon that includes both a single-domain and a truncated haemoglobin. Mol Microbiol. 57:735-750.
16. Flint DH, Smyk-Randall E, Tuminello JF, Draczynska-Lusiak B, Brown OR. 1993. The inactivation of dihydroxy-acid dehydratase in Escherichia coli treated with hyperbaric oxygen occurs because of the destruction of its Fe-S cluster, but the enzyme remains in the cell in a form that can be reactivated. J Biol Chem. 268:25547-25552.
17. Fouts DE, et al. 2005. Major structural differences and novel potential virulence mechanisms from the genomes of multiple campylobacter species. PLoS Biol. 3:e15.
18. Frazzon J, Fick JR, Dean DR. 2002. Biosynthesis of iron-sulphur clusters is a complex and highly conserved process. Biochem Soc Trans. 30:680-685.
19. Gaynor EC, et al. 2004. The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J Bacteriol. 186:503-517.
20. Gibreel A, et al. 2004. Incidence of antibiotic resistance in Campylobacter jejuni isolated in Alberta, Canada, from 1999 to 2002, with special reference to tet (O)-mediated tetracycline resistance. Antimicrob Agents Chemother. 48:3442-3450.
21. Gilbert M, et al. 2002. The genetic bases for the variation in the lipooligosaccharide of the mucosal pathogen, Campylobacter jejuni. Biosynthesis of sialylated ganglioside mimics in the core oligosaccharide. J Biol Chem. 277:327-337.
22. Grogono-Thomas R, Blaser MJ, Ahmadi M, Newell DG. 2003. Role of S-layer protein antigenic diversity in the immune responses of sheep experimentally challenged with Campylobacter fetus subsp. fetus. Infect Immun. 71:147-154.
23. Guccione E, et al. 2008. Amino acid-dependent growth of Campylobacter jejuni: key roles for aspartase (AspA) under microaerobic and oxygen-limited conditions and identification of AspB (Cj0762), essential for growth on glutamate. Mol Microbiol. 69:77-93.
24. Guerry P, et al. 2012. Campylobacter polysaccharide capsules: virulence and vaccines. Front Cell Infect Microbiol. 2:7.
25. Gundogdu O, et al. 2007. Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 8:162.
26. Hendrixson DR, DiRita VJ. 2004. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol. 52:471-484.
27. Hofreuter D, Novik V, Galan JE. 2008. Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell Host Microbe. 4:425-433.
28. Howard SL, et al. 2009. Campylobacter jejuni glycosylation island important in cell charge, legionaminic acid biosynthesis, and colonization of chickens. Infect Immun. 77:2544-2556.
29. Janvier B, et al. 1998. Characterization and gene sequencing of a 19-kDa periplasmic protein of Campylobacter jejuni/coli. Res Microbiol. 149:95-107.
30. Karlyshev AV, Linton D, Gregson NA, Lastovica AJ, Wren BW. 2000. Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol Microbiol. 35:529-541.
31. Karlyshev AV, et al. 2005. Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses. Mol Microbiol. 55:90-103.
32. Kirkbride CA. 1993. Diagnoses in 1, 784 ovine abortions and stillbirths. J Vet Diagn Invest. 5:398-402.
33. Kurtz S, et al. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:R12.
34. Lam WW, et al. 2010. Molecular interaction of flagellar export chaperone FliS and cochaperone HP1076 in Helicobacter pylori. FASEB J. 24:4020-4032.
35. Lastovica A. 1996. Campylobacter/Helicobacter bacteremia in Cape Town, South Africa 1977-1995. In: Newell DG, Ketley JM, Feldman RA, editors. Campylobacters, helicobacters, and related organisms. New York: Plenum Press. p. 475-479.
36. Lastovica A, Skirrow M. 2000. Clinical significance of Campylobacter and related species other than Campylobacter jejuni and C. coli. In: Nachamkin I, Blaser MJ, editors. Campylobacter. Washington (DC): ASM Press. p. 89-120.
37. Le Gall T, Darlu P, Escobar-Paramo P, Picard B, Denamur E. 2005. Selection-driven transcriptome polymorphism in Escherichia coli/Shigella species. Genome Res. 15:260-268.
38. Leach S, Harvey P, Wali R. 1997. Changes with growth rate in the membrane lipid composition of and amino acid utilization by continuous cultures of Campylobacter jejuni. J Appl Microbiol. 82:631-640.
39. Leon-Kempis Mdel R, Guccione E, Mulholland F, Williamson MP, Kelly DJ. 2006. The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol Microbiol. 60:1262-1275.
40. 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.
41. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 25:402-408.
42. Malik-Kale P, et al. 2007. Characterization of genetically matched isolates of Campylobacter jejuni reveals that mutations in genes involved in flagellar biosynthesis alter the organism's virulence potential. Appl Environ Microbiol. 73:3123-3136.
43. Margulies M, et al. 2005. Genome sequencing in microfabricated highdensity picolitre reactors. Nature 437:376-380.
44. McNally DJ, 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.
45. Miller WG, Parker CT, Heath S, Lastovica AJ. 2007. Identification of genomic differences between Campylobacter jejuni subsp. jejuni and C. jejuni subsp. doylei at the nap locus leads to the development of a C. jejuni subspeciation multiplex PCR method. BMC Microbiol. 7:11.
46. Miller CE, Williams PH, Ketley JM. 2009. Pumping iron: mechanisms for iron uptake by Campylobacter. Microbiology 155:3157-3165.
47. Morey F. 1996. Five years of Campylobacter bacteremia in central Australia. In: Newell DG, Ketley JM, Feldman RA, editors. Campylobacters, helicobacters, and related organisms. New York: Plenum Press. p. 491-494.
48. Nachamkin I, Allos BM, Ho T. 1998. Campylobacter species and Guillain-Barre syndrome. Clin Microbiol Rev. 11:555-567.
49. Ogden ID, et al. 2009. Campylobacter excreted into the environment by animal sources: prevalence, concentration shed, and host association. Foodborne Pathog Dis. 6:1161-1170.
50. Page RD. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 12:357-358.
51. Palyada K, Threadgill D, Stintzi A. 2004. Iron acquisition and regulation in Campylobacter jejuni. J Bacteriol. 186:4714-4729.
52. Palyada K, et al. 2009. Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. BMC Genomics 10:481.
53. Parker CT, Miller WG, Horn ST, Lastovica AJ. 2007. Common genomic features of Campylobacter jejuni subsp. doylei strains distinguish them from C. jejuni subsp. jejuni. BMC Microbiol. 7:50.
54. Parker CT, Quinones B, Miller WG, Horn ST, Mandrell RE. 2006. Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C-jejuni strain RM1221. J Clin Microbiol. 44:4125-4135.
55. Parker CT, et al. 2005. Comparison of Campylobacter jejuni lipooligosaccharide biosynthesis loci from a variety of sources. J Clin Microbiol. 43:2771-2781.
56. Peterson MC. 1994. Clinical aspects of Campylobacter jejuni infections in adults. West J Med. 161:148-152.
57. Poly F, et al. 2007. Heterogeneity of a Campylobacter jejuni protein that is secreted through the flagellar filament. Infect Immun. 75:3859-3867.
58. Poly F, et al. 2008. Characterization of two Campylobacter jejuni strains for use in volunteer experimental-infection studies. Infect Immun. 76:5655-5667.
59. Ridley KA, Rock JD, Li Y, Ketley JM. 2006. Heme utilization in Campylobacter jejuni. J Bacteriol. 188:7862-7875.
60. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 132:365-386.
61. Sahin O, et al. 2008. Emergence of a tetracycline-resistant Campylobacter jejuni clone associated with outbreaks of ovine abortion in the United States. J Clin Microbiol. 46:1663-1671.
62. Sahin O, et al. 2012. Molecular evidence for zoonotic transmission of an emergent, highly pathogenic Campylobacter jejuni clone in the United States. J Clin Microbiol. 50:680-687.
63. Santos SR, Ochman H. 2004. Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ Microbiol. 6:754-759.
64. Schoenhofen IC, et al. 2006. Functional characterization of dehydratase/aminotransferase pairs from Helicobacter and Campylobacter: enzymes distinguishing the pseudaminic acid and bacillosamine biosynthetic pathways. J Biol Chem. 281:723-732.
65. Seal BS, et al. 2007. Proteomic analyses of a robust versus a poor chicken gastrointestinal colonizing isolate of Campylobacter jejuni. J Proteome Res. 6:4582-4591.
66. Siboo IR, Chaffin DO, Rubens CE, Sullam PM. 2008. Characterization of the accessory Sec system of Staphylococcus aureus. J Bacteriol. 190:6188-6196.
67. Skirrow MB. 1994. Diseases due to Campylobacter, Helicobacter and related bacteria. J Comp Pathol. 111:113-149.
68. Smyth GK. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 3: Article3.
69. Stahl M, Butcher J, Stintzi A. 2012. Nutrient acquisition and metabolism by Campylobacter jejuni. Front Cell Infect Microbiol. 2:5.
70. Stahl M, et al. 2011. L-Fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci U S A. 108:7194-7199.
71. Tauxe RV. 1997. Emerging foodborne diseases: an evolving public health challenge. Emerg Infect Dis. 3:425-434.
72. Thomas MT, et al. 2011. Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on L-lactate. Environ Microbiol. 13:48-61.
73. van Putten JP, van Alphen LB, Wosten MM, de Zoete MR. 2009. Molecular mechanisms of Campylobacter infection. Curr Top Microbiol Immunol. 337:197-229.
74. van Vliet AHM, Baillon MLA, Penn CW, Ketley JM. 2001. The iron-induced ferredoxin FdxA of Campylobacter jejuni is involved in aerotolerance. FEMS Microbiol Lett. 196:189-193.
75. van Vliet AH, Rock JD, Madeleine LN, Ketley JM. 2000. The iron-responsive regulator Fur of Campylobacter jejuni is expressed from two separate promoters. FEMS Microbiol Lett. 188:115-118.
76. Velayudhan J, Jones MA, Barrow PA, Kelly DJ. 2004. L-serine catabolism via an oxygen-labile L-serine dehydratase is essential for colonization of the avian gut by Campylobacter jejuni. Infect Immun. 72:260-268.
77. Wassenaar TM, Fry BN, van der Zeijst BA. 1995. Variation of the flagellin gene locus of Campylobacter jejuni by recombination and horizontal gene transfer. Microbiology 141(Pt 1):95-101.
78. Weerakoon DR, Borden NJ, Goodson CM, Grimes J, Olson JW. 2009. The role of respiratory donor enzymes in Campylobacter jejuni host colonization and physiology. Microb Pathog. 47:8-15.
79. Weerakoon DR, Olson JW. 2008. The Campylobacter jejuni NADH: ubiquinone oxidoreductase (complex I) utilizes flavodoxin rather than NADH. J Bacteriol. 190:915-925.
80. Weingarten RA, Grimes JL, Olson JW. 2008. Role of Campylobacter jejuni respiratory oxidases and reductases in host colonization. Appl Environ Microbiol. 74:1367-1375.
81. Yamasaki M, Igimi S, Katayama Y, Yamamoto S, Amano F. 2004. Identification of an oxidative stress-sensitive protein from Campylobacter jejuni, homologous to rubredoxin oxidoreductase/rubrerythrin. FEMS Microbiol Lett. 235:57-63.
82. Zeng X, Xu F, Lin J. 2009. Molecular, antigenic, and functional characteristics of ferric enterobactin receptor CfrA in Campylobacter jejuni. Infect Immun. 77:5437-5448.