Competing isogenic Campylobacter strains exhibit variable population structures in vivo

Applied and Environmental Microbiology

Volumn 74, Issue 12, 2008, Pages 3857-3867

  Coward, Chris ^a   Van Diemen, Pauline M ^b   Conlan, Andrew J K ^c   Gog, Julia R ^c   Stevens, Mark P ^b   Jones, Michael A ^d   Maskell, Duncan J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; PLANNING; RISK PERCEPTION; STRATEGIC PLANNING;

(E ,3E) PROCESS; AMERICAN SOCIETY; CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; CONFOUNDING FACTORS; CONTROL STRATEGIES; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT (GIT); IN-VIVO; MONITOR (CO); PHENOTYPIC DIFFERENCES; PHENOTYPIC VARIATIONS; POPULATION LEVELS; POPULATION STRUCTURES; RELATIVE AMOUNTS; RISK FACTORS; SIGNATURE-TAGGED MUTAGENESIS (STM); SIMPLE MODELING; WILD-TYPE (WT); WILD-TYPE BACTERIA;

EXPERIMENTS;

BACTERIAL DISEASE; BACTERIUM; COLONIZATION; DISEASE TRANSMISSION; POPULATION STRUCTURE; POULTRY;

ADOLESCENT; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM MUTANT; BIRD; CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; GASTROINTESTINAL DISEASE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POPULATION STRUCTURE;

ANIMALS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CECUM; CHICKENS; CHROMOSOMES, BACTERIAL; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

AVES; CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; GALLUS GALLUS;

EID: 45749100950     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02835-07     Document Type: Article

References (41)

1. Adkin, A., E. Hartnett, L. Jordan, D. Newell, and H. Davison. 2006. Use of a systematic review to assist the development of Campylobacter control strategies in broilers. J. Appl. Microbiol. 100:306-315.
2. Beery, J. T., M. B. Hugdahl, and M. P. Doyle. 1988. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microbiol. 54:2365-2370.
3. Cawthraw, S. A., T. M. Wassenaar, R. Ayling, and D. G. Newell. 1996. Increased colonization potential of Campylobacter jejuni strain 81116 after passage through chickens and its implication on the rate of transmission within flocks. Epidemiol. Infect. 117:213-215.
4. Chen, H.-C., and N. J. Stern. 2001. Competitive exclusion of heterologous Campylobacter spp. in chicks. Appl. Environ. Microbiol. 67:848-851.
5. Conlan, A. J. K., C. Coward, A. J. Grant, D. J. Maskell, and J. R. Gog. 2007. Campylobacter jejuni colonization and transmission in broiler chickens: a modelling perspective. J. R. Soc. Interface 4:819-829.
6. El-Shibiny, A., P. L. Connerton, and I. F. Connerton. 2007. Campylobacter succession in broiler chickens. Vet. Microbiol. 125:323-332.
7. Fouts, D. E., E. F. Mongodin, R. E. Mandrell, W. G. Miller, D. A. Rasko, J. Ravel, L. M. Brinkac, R. T. DeBoy, C. T. Parker, S. C. Daugherty, R. J. Dodson, A. S. Durkin, R. Madupu, S. A. Sullivan, J. U. Shetty, M. A. Ayodeji, A. Shvartsbeyn, M. C. Schatz, J. H. Badger, C. M. Fraser, and K. E. Nelson. 2005. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol. 3:e15. doi:10.1371/journal.pbio.0030015.
8. Gilbert, M., M. F. Karwaski, S. Bernatchez, N. M. Young, E. Taboada, J. Michniewicz, A. M. Cunningham, and W. W. Wakarchuk. 2002. The genetic bases for the variation in the lipo-oligosaccharide of the mucosal pathogen Campylobacter jejuni. Biosynthesis of sialylated ganglioside mimics in the core oligosaccharide. J. Biol. Chem. 277:327-337.
9. Grant, A. J., C. Coward, M. A. Jones, C. A. Woodall, P. A. Barrow, and D. J. Maskell. 2005. Signature-tagged transposon mutagenesis studies demonstrate the dynamic nature of cecal colonization of 2-week-old chickens by Campylobacter jejuni. Appl. Environ. Microbiol. 71:8031-8041.
10. Guerry, P., C. M. Szymanski, M. M. Prendergast, T. E. Hickey, C. P. Ewing, D. L. Pattarini, and A. P. Moran. 2002. Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect. Immun. 70:787-793.
11. Gundogdu, O., S. D. Bentley, M. T. Holden, H. Parkhill, N. Dorrell, and B. W. Wren. 2007. Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 8:doi:10.1186/1471- 2164-8-162.
12. Health Protection Agency. 2006. Campylobacter spp. Laboratory reports of faecal isolates England & Wales, 1986-2005. Health Protection Agency, United Kingdom. http://www.hpa.org.uk/infections/topics_az/ campy/data_ew.htm.
13. Hendrixson, D. R., and V. J. DiRita. 2004. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52:471-484.
14. Humphrey, T., S. O'Brien, and M. Madsen. 2007. Campylobacters as zoonotic pathogens: a food production perspective. Int. J. Food Microbiol. 117:237-257.
15. Inglis, G. D., and L. D. Kalischuk. 2004. Direct quantification of Campylobacter jejuni and Campylobacter lanienae in feces of cattle by real-time quantitative PCR. Appl. Environ. Microbiol. 70:2296-2306.
16. Jones, M. A., K. L. Marston, C. A. Woodall, D. J. Maskell, D. Linton, A. V. Karlyshev, N. Dorrell, B. W. Wren, and P. A. Barrow. 2004. Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 72:3769-3776.
17. 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.
18. Karlyshev, A. V., and B. W. Wren. 2005. Development and application of an insertional system for gene delivery and expression in Campylobacter jejuni. Appl. Environ. Microbiol. 71:4004-4013.
19. Konkel, M. E., J. E. Christensen, A. S. Dhillon, A. B. Lane, R. Hare-Sanford, D. M. Schaberg, and C. L. Larson. 2007. Campylobacter jejuni strains compete for colonization in broiler chicks. Appl. Environ. Microbiol. 73:2297-2305.
20. Levinson, G., and G. A. Gutman. 1987. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol. Biol. Evol. 4:203-221.
21. Linton, D., A. V. Karlyshev, and B. W. Wren. 2001. Deciphering Campylobacter jejuni cell surface interactions from the genome sequence. Curr. Opp. Microbiol. 4:35-40.
22. Luo, N., S. Pereira, O. Sahin, J. Lin, S. Huang, L. Michel, and Q. Zhang. 2005. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl. Acad. Sci. USA 102:541-546.
23. Mazurkiewicz, P., C. M. Tang, C. Boone, and D. W. Holden. 2006. Signature-tagged mutagenesis: barcoding mutants for genome-wide screens. Nat. Rev. Genet. 7:929-939.
24. Morgan, E., J. D. Campbell, S. C. Rowe, J. Bispham, M. P. Stevens, A. J. Bowen, P. A. Barrow, D. J. Maskell, and T. S. Wallis. 2004. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol. Gen. Genet. 54:994-1010.
25. Naikare, H., K. Palyada, R. Panciera, D. Marlow, and A. Stinzi. 2006. Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect. Immun. 74:5433-5444.
26. Park, S. F., D. Purdy, and S. Leach. 2000. Localized reversible frameshift mutation in the flhA gene confers phase variability to flagellin expression in Campylobacter coli. J. Bacteriol. 182:207-210.
27. Parkhill, J., B. W. Wren, K. Mingall, J. M. Ketley, C. Churcher, D. Basham, T. Chillingworth, R. M. Davies, T. Feltwell, S. Holroyd, K. Jagels, A. V. Karlyshev, S. Moule, M. J. Pallen, C. W. Penn, M. A. Quail, M. A. Rajandream, K. M. Rutherford, A. H. van Vliet, S. Whitehead, and B. G. Barrell. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
28. Poly, F., T. Read, D. R. Tribble, S. Baqar, M. Lorenzo, and P. Guerry. 2007. Genome sequence of a clinical isolate of Campylobacter jejuni from Thailand. Infect. Immun. 75:3425-3433.
29. Ringoir, D. D., and V. Korolik. 2003. Colonisation phenotype and colonisation potential differences in Campylobacter jejuni strains in chickens before and after passage in vivo. Vet. Microbiol. 92:225-325.
30. Ringoir, D. D., D. Szylo, and V. Korolik. 2007. Comparison of 2-day-old and 14-day-old chicken colonization models for Campylobacter jejuni. FEMS Immunol. Med. Microbiol. 49:155-158.
31. Sambrook, J., and D. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Scott, A. E., A. R. Timms, P. L. Connerton, A. El-Shibiny, and I. F. Connerton. 2007. Bacteriophage influence Campylobacter jejuni types populating broiler chickens. Environ. Microbiol. 9:2341-2353.
33. Skånseng, B., P. Trosvik, M. Zimonja, G. Johnsen, L. Bjerrum, K. Pedersen, N. Wallin, and K. Rudi. 2007. Co-infection dynamics of a major food-borne zoonotic pathogen in chicken. PLoS Pathog. 3:e175. doi:10.1371/journal .ppat. 0030175.
34. Stintzi, A., D. Marlow, K. Palyada, H. Naikare, R. Panciera, L. Whitworth, and C. Clarke. 2005. Use of genome-wide expression profiling and mutagenesis to study the intestinal lifestyle of Campylobacter jejuni. Infect. Immun. 73:1797-1810.
35. Szymanski, C. M., F. St. Michael, H. C. Jarrell, J. Li, M. Gilbert, S. Larocque, E. Vinogradov, and J.-R. Brisson. 2003. Detection of conserved N-linked glycans and phase-variable lipooligosaccharides and capsules from Campylobacter cells by mass spectrometry and high resolution magic angle spinning NMR spectroscopy. J. Biol. Chem. 278:24509-24520.
36. van Vliet, A. H. M., A. C. Wood, J. Henderson, K. Wooldridge, and J. M. Ketley. 1997. Genetic manipulation of enteric Campylobacter species. Methods Microbiol. 27:407-419.
37. Wassenaar, T. M., J. A. Wagenaar, A. Rigter, C. Fearnley, D. G. Newell, and B. Duim. 2002. Homonucleotide stretches in chromosomal DNA of Campylobacter jejuni display high frequency polymorphism as detected by direct PCR analysis. FEMS Microbiol. Lett. 212:77-85.
38. Watson, R. O., V. Novik, D. Hofreuter, M. Lara-Tejero, and J. E. Galán. 2007. A MyD88-deficient mouse model reveals a role for Nramp1 in Campylobacter jejuni infection. Infect. Immun. 75:1994-2003.
39. Yao, R., R. A. Alm, T. J. Trust, and P. Guerry. 1993. Construction of new Campylobacter cloning vectors and a new mutational cat cassette. Gene 130:127-130.
40. Yao, R., D. H. Burr, and P. Guerry. 1997. CheY-mediated modulation of Campylobacter jejuni virulence. Mol. Microbiol. 23:1021-1031.
41. Young, K. T., L. M. Davis, and V. DiRita. 2007. Campylobacter jejuni: molecular biology and pathogenesis. Nat. Rev. Microbiol. 5:665-679.