Role of environmental survival in transmission of Campylobacter jejuni

FEMS Microbiology Letters

Volumn 356, Issue 1, 2014, Pages 8-19

  Bronowski, Christina ^a   James, Chloe E ^b   Winstanley, Craig ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF SALFORD   (United Kingdom)

Author keywords

Campylobacter; Environment; Gastroenteritis; Zoonosis

Indexed keywords

OXYGEN; WATER;

AGRICULTURAL LAND; ARTICLE; BACTERIAL GENOME; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL TRANSMISSION; BACTERIAL VIABILITY; BIOFILM; CAMPYLOBACTER JEJUNI; CAMPYLOBACTERIOSIS; DISEASE CARRIER; ENVIRONMENT; GENETIC VARIABILITY; GENOTYPE; HUMAN; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUTRIENT; ORGANISMAL INTERACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PSEUDOMONAS; QUORUM SENSING; VIABLE BUT NONCULTURABLE STATE; WILDLIFE; ZOONOSIS; ANIMAL; BACTERIAL GENE; GASTROENTERITIS; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY; TRANSMISSION;

ANIMALIA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CAMPYLOBACTER JEJUNI;

ANIMALS; BIOFILMS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; ENVIRONMENTAL MICROBIOLOGY; GASTROENTERITIS; GENES, BACTERIAL; HUMANS; MICROBIAL INTERACTIONS; MICROBIAL VIABILITY;

EID: 84903890360     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12488     Document Type: Article

References (135)

1. Abe T, Haga S, Yokoyama K & Watanabe N (2008) An outbreak of Campylobacter jejuni subsp. jejuni infection via tap water. Jpn J Infect Dis 61: 327.
2. Ahmed MU, Dunn L & Ivanova EP (2012) Evaluation of current molecular approaches for genotyping of Campylobacter jejuni strains. Foodborne Pathog Dis 9: 375-385.
3. Andersen MT, Brondsted L, Pearson BM, Mulholland F, Parker M, Pin C, Wells JM & Ingmer H (2005) Diverse roles for HspR in Campylobacter jejuni revealed by the proteome, transcriptome and phenotypic characterization of an hspR mutant. Microbiology 151: 905-915.
4. Arnaut-Rollier I, De Zutter L & Van Hoof J (1999) Identities of the Pseudomonas spp. in flora from chilled chicken. Int J Food Microbiol 48: 87-96.
5. Asakura H, Yamasaki M, Yamamoto S & Igimi S (2007) Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni. FEMS Microbiol Lett 275: 278-285.
6. Atack JM & Kelly DJ (2008) Contribution of the stereospecific methionine sulphoxide reductases MsrA and MsrB to oxidative and nitrosative stress resistance in the food-borne pathogen Campylobacter jejuni. Microbiology 154: 2219-2230.
7. Atack JM & Kelly DJ (2009) Oxidative stress in Campylobacter jejuni: responses, resistance and regulation. Future Microbiol 4: 677-690.
8. Auld H, MacIver D & Klaassen J (2004) Heavy rainfall and waterborne disease outbreaks: the Walkerton example. J Toxicol Environ Health A 67: 1879-1887.
9. Axelsson-Olsson D, Waldenstrom J, Broman T, Olsen B & Holmberg M (2005) Protozoan Acanthamoeba polyphaga as a potential reservoir for Campylobacter jejuni. Appl Environ Microbiol 71: 987-992.
10. Baffone W, Casaroli A, Citterio B, Pierfelici L, Campana R, Vittoria E, Guaglianone E & Donelli G (2006) Campylobacter jejuni loss of culturability in aqueous microcosms and ability to resuscitate in a mouse model. Int J Food Microbiol 107: 83-91.
11. Baillon ML, van Vliet AH, Ketley JM, Constantinidou C & Penn CW (1999) An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J Bacteriol 181: 4798-4804.
12. Bare J, Houf K, Verstraete T, Vaerewijck M & Sabbe K (2011) Persistence of free-living protozoan communities across rearing cycles in commercial poultry houses. Appl Environ Microbiol 77: 1763-1769.
13. Barer MR & Harwood CR (1999) Bacterial viability and culturability. Adv Microb Physiol 41: 93-137.
14. Beumer RR, de Vries J & Rombouts FM (1992) Campylobacter jejuni non-culturable coccoid cells. Int J Food Microbiol 15: 153-163.
15. Biggs PJ, Fearnhead P, Hotter G, Mohan V, Collins-Emerson J, Kwan E, Besser TE, Cookson A, Carter PE & French NP (2011) Whole-genome comparison of two Campylobacter jejuni isolates of the same sequence type reveals multiple loci of different ancestral lineage. PLoS One 6: e27121.
16. Brondsted L, Andersen MT, Parker M, Jorgensen K & Ingmer H (2005) The HtrA protease of Campylobacter jejuni is required for heat and oxygen tolerance and for optimal interaction with human epithelial cells. Appl Environ Microbiol 71: 3205-3212.
17. Buswell CM, Herlihy YM, Lawrence LM, McGuiggan JT, Marsh PD, Keevil CW & Leach SA (1998) Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and -rRNA staining. Appl Environ Microbiol 64: 733-741.
18. Cabiscol E, Tamarit J & Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3: 3-8.
19. Candon HL, Allan BJ, Fraley CD & Gaynor EC (2007) Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J Bacteriol 189: 8099-8108.
20. Champion OL, Gaunt MW, Gundogdu O, Elmi A, Witney AA, Hinds J, Dorrell N & Wren BW (2005) Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source. P Natl Acad Sci USA 102: 16043-16048.
21. Clark CG, Price L, Ahmed R, Woodward DL, Melito PL, Rodgers FG, Jamieson F, Ciebin B, Li A & Ellis A (2003) Characterization of waterborne outbreak-associated Campylobacter jejuni, Walkerton, Ontario. Emerg Infect Dis 9: 1232-1241.
22. Clark CG, Bryden L, Cuff WR, Johnson PL, Jamieson F, Ciebin B & Wang G (2005) Use of the oxford multilocus sequence typing protocol and sequencing of the flagellin short variable region to characterize isolates from a large outbreak of waterborne Campylobacter sp. strains in Walkerton, Ontario, Canada. J Clin Microbiol 43: 2080-2091.
23. Colles FM, Jones K, Harding RM & Maiden MC (2003) Genetic diversity of Campylobacter jejuni isolates from farm animals and the farm environment. Appl Environ Microbiol 69: 7409-7413.
24. Cools I, Uyttendaele M, Caro C, D'Haese E, Nelis HJ & Debevere J (2003) Survival of Campylobacter jejuni strains of different origin in drinking water. J Appl Microbiol 94: 886-892.
25. Day WA Jr, Sajecki JL, Pitts TM & Joens LA (2000) Role of catalase in Campylobacter jejuni intracellular survival. Infect Immun 68: 6337-6345.
26. Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, Bootsma HJ, Willems RJ, Urwin R & Maiden MC (2001) Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39: 14-23.
27. Dingle KE, Colles FM, Falush D & Maiden MC (2005) Sequence typing and comparison of population biology of Campylobacter coli and Campylobacter jejuni. J Clin Microbiol 43: 340-347.
28. Dingle KE, McCarthy ND, Cody AJ, Peto TE & Maiden MC (2008) Extended sequence typing of Campylobacter spp., United Kingdom. Emerg Infect Dis 14: 1620-1622.
29. Dorrell N & Wren BW (2007) The second century of Campylobacter research: recent advances, new opportunities and old problems. Curr Opin Infect Dis 20: 514-518.
30. Dorrell N, Mangan JA, Laing KG 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.
31. Dorrell N, Hinchliffe SJ & Wren BW (2005) Comparative phylogenomics of pathogenic bacteria by microarray analysis. Curr Opin Microbiol 8: 620-626.
32. Fields JA & Thompson SA (2008) Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J Bacteriol 190: 3411-3416.
33. Flint A, Sun YQ & Stintzi A (2012) Cj1386 is an ankyrin-containing protein involved in heme trafficking to catalase in Campylobacter jejuni. J Bacteriol 194: 334-345.
34. Fouts DE, Mongodin EF, Mandrell RE et al. (2005) Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 3: e15.
35. French N, Barrigas M, Brown P, Ribiero P, Williams N, Leatherbarrow H, Birtles R, Bolton E, Fearnhead P & Fox A (2005) Spatial epidemiology and natural population structure of Campylobacter jejuni colonizing a farmland ecosystem. Environ Microbiol 7: 1116-1126.
36. Gangaiah D, Kassem II, Liu Z & Rajashekara G (2009) Importance of polyphosphate kinase 1 for Campylobacter jejuni viable-but-nonculturable cell formation, natural transformation, and antimicrobial resistance. Appl Environ Microbiol 75: 7838-7849.
37. Gangaiah D, Liu Z, Arcos J, Kassem II, Sanad Y, Torrelles JB & Rajashekara G (2010) Polyphosphate kinase 2: a novel determinant of stress responses and pathogenesis in Campylobacter jejuni. PLoS One 5: e12142.
38. Garenaux A, Guillou S, Ermel G, Wren B, Federighi M & Ritz M (2008) Role of the Cj1371 periplasmic protein and the Cj0355c two-component regulator in the Campylobacter jejuni NCTC 11168 response to oxidative stress caused by paraquat. Res Microbiol 159: 718-726.
39. Gaynor EC, Wells DH, MacKichan JK & Falkow S (2005) The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol Microbiol 56: 8-27.
40. Gonzalez M & Hanninen ML (2012) Effect of temperature and antimicrobial resistance on survival of Campylobacter jejuni in well water: application of the Weibull model. J Appl Microbiol 113: 284-293.
41. Gubbels SM, Kuhn KG, Larsson JT, Adelhardt M, Engberg J, Ingildsen P, Hollesen LW, Muchitsch S, Mølbak K & Ethelberg S (2012) A waterborne outbreak with a single clone of Campylobacter jejuni in the Danish town of Køge in May 2010. Scand J Infect Dis 44: 586-594.
42. Guccione E, Leon-Kempis Mdel R, Pearson BM, Hitchin E, Mulholland F, van Diemen PM, Stevens MP & Kelly DJ (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.
43. Gundogdu O, Mills DC, Elmi A, Martin MJ, Wren BW & Dorrell N (2011) The Campylobacter jejuni transcriptional regulator Cj1556 plays a role in the oxidative and aerobic stress response and is important for bacterial survival in vivo. J Bacteriol 193: 4238-4249.
44. Gundogdu O, Wren BW & Dorrell N (2014) Genetic Mechanisms Involved in Campylobacter jejuni Survival Under Oxidative Stress Conditions Campylobacter Ecology and Evolution, (Sheppard SK, Ed). Caister Academic Press, Norfolk, UK.
45. Hald B, Knudsen K, Lind P & Madsen M (2001) Study of the infectivity of saline-stored Campylobacter jejuni for day-old chicks. Appl Environ Microbiol 67: 2388-2392.
46. Hanning I, Jarquin R & Slavik M (2008) Campylobacter jejuni as a secondary colonizer of poultry biofilms. J Appl Microbiol 105: 1199-1208.
47. Hazeleger WC, Janse JD, Koenraad PM, Beumer RR, Rombouts FM & Abee T (1995) Temperature-dependent membrane fatty acid and cell physiology changes in coccoid forms of Campylobacter jejuni. Appl Environ Microbiol 61: 2713-2719.
48. Hepworth PJ, Ashelford KE, Hinds J et al. (2011) Genomic variations define divergence of water/wildlife-associated Campylobacter jejuni niche specialists from common clonal complexes. Environ Microbiol 13: 1549-1560.
49. Hilbert F, Scherwitzel M, Paulsen P & Szostak MP (2010) Survival of Campylobacter jejuni under conditions of atmospheric oxygen tension with the support of Pseudomonas spp. Appl Environ Microbiol 76: 5911-5917.
50. Hofreuter D, Tsai J, Watson RO et al. (2006) Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun 74: 4694-4707.
51. Hofreuter D, Novik V & Galan JE (2008) Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell Host Microbe 4: 425-433.
52. Humphrey T, O'Brien S & Madsen M (2007) Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117: 237-257.
53. Hwang S, Kim M, Ryu S & Jeon B (2011) Regulation of oxidative stress response by CosR, an essential response regulator in Campylobacter jejuni. PLoS One 6: e22300.
54. Ica T, Caner V, Istanbullu O, Nguyen HD, Ahmed B, Call DR & Beyenal H (2012) Characterization of mono- and mixed-culture Campylobacter jejuni biofilms. Appl Environ Microbiol 78: 1033-1038.
55. Jang KI, Kim MG, Ha SD, Kim KS, Lee KH, Chung DH, Kim CH & Kim KY (2007) Morphology and adhesion of Campylobacter jejuni to chicken skin under varying conditions. J Microbiol Biotechnol 17: 202-206.
56. Jolley KA & Maiden MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11: 595.
57. Joshua GWP, Guthrie-Irons C, Karlyshev AV & Wren BW (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152: 387-396.
58. Kalmokoff M, Lanthier P, Tremblay TL, Foss M, Lau PC, Sanders G, Austin J, Kelly J & Szymanski CM (2006) Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188: 4312-4320.
59. Karagiannis I, Sideroglou T, Gkolfinopoulou K, Tsouri A, Lampousaki D, Velonakis EN, Scoulica EV, Mellou K, Panagiotopoulos T & Bonovas S (2010) A waterborne Campylobacter jejuni outbreak on a Greek island. Epidemiol Infect 138: 1726-1734.
60. Karenlampi R, Rautelin H, Schonberg-Norio D, Paulin L & Hanninen ML (2007) Longitudinal study of Finnish Campylobacter jejuni and C. coli isolates from humans, using multilocus sequence typing, including comparison with epidemiological data and isolates from poultry and cattle. Appl Environ Microbiol 73: 148-155.
61. Kassem II & Rajashekara G (2011) An ancient molecule in a recalcitrant pathogen: the contributions of poly-P to the pathogenesis and stress responses of Campylobacter jejuni. Future Microbiol 6: 1117-1120.
62. Kelly DJ (2001) The physiology and metabolism of Campylobacter jejuni and Helicobacter pylori. Symp Ser Soc Appl Microbiol 90: 16S-24S.
63. Klancnik A, Botteldoorn N, Herman L & Mozina SS (2006) Survival and stress induced expression of groEL and rpoD of Campylobacter jejuni from different growth phases. Int J Food Microbiol 112: 200-207.
64. Kuusi M, Klemets P, Miettinen I, Laaksonen I, Sarkkinen H, Hanninen ML, Rautelin H, Kela E & Nuorti JP (2004) An outbreak of gastroenteritis from a non-chlorinated community water supply. J Epidemiol Community Health 58: 273-277.
65. Lazaro B, Carcamo J, Audicana A, Perales I & Fernandez-Astorga A (1999) Viability and DNA maintenance in nonculturable spiral Campylobacter jejuni cells after long-term exposure to low temperatures. Appl Environ Microbiol 65: 4677-4681.
66. Lehtola MJ, Pitkanen T, Miebach L & Miettinen IT (2006) Survival of Campylobacter jejuni in potable water biofilms: a comparative study with different detection methods. Water Sci Technol 54: 57-61.
67. Leonard EE, Takata T, Blaser MJ, Falkow S, Tompkins LS & Gaynor EC (2003) Use of an open-reading frame-specific Campylobacter jejuni DNA microarray as a new genotyping tool for studying epidemiologically related isolates. J Infect Dis 187: 691-694.
68. Levesque S, Frost E, Arbeit RD & Michaud S (2008) Multilocus sequence typing of Campylobacter jejuni isolates from humans, chickens, raw milk, and environmental water in Quebec, Canada. J Clin Microbiol 46: 3404-3411.
69. Lind L, Sjogren E, Melby K & Kaijser B (1996) DNA fingerprinting and serotyping of Campylobacter jejuni isolates from epidemic outbreaks. J Clin Microbiol 34: 892-896.
70. Maal-Bared R, Bartlett KH, Bowie WR & Hall ER (2012) Campylobacter spp. distribution in biofilms on different surfaces in an agricultural watershed (Elk Creek, British Columbia): using biofilms to monitor for Campylobacter. Int J Hyg Environ Health 215: 270-278.
71. Manning G, Dowson CG, Bagnall MC, Ahmed IH, West M & Newell DG (2003) Multilocus sequence typing for comparison of veterinary and human isolates of Campylobacter jejuni. Appl Environ Microbiol 69: 6370-6379.
72. McCarthy ND, Colles FM, Dingle KE, Bagnall MC, Manning G, Maiden MC & Falush D (2007) Host-associated genetic import in Campylobacter jejuni. Emerg Infect Dis 13: 267-272.
73. McCarthy ND, Gillespie IA, Lawson AJ, Richardson J, Neal KR, Hawtin PR, Maiden MCJ & O'Brien SJ (2012) Molecular epidemiology of human Campylobacter jejuni shows association between seasonal and international patterns of disease. Epidemiol Infect 140: 2247-2255.
74. Medema GJ, Schets FM, van de Giessen AW & Havelaar AH (1992) Lack of colonization of 1 day old chicks by viable, non-culturable Campylobacter jejuni. J Appl Bacteriol 72: 512-516.
75. Miller WG, On SLW, Wang G, Fontanoz S, Lastovica AJ & Mandrell RE (2005) Extended multilocus sequence typing system for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus. J Clin Microbiol 43: 2315-2329.
76. Moore JE (2001) Bacterial dormancy in Campylobacter: abstract theory or cause for concern? Int J Food Sci Technol 36: 593-600.
77. Moran AP & Upton ME (1986) A comparative study of the rod and coccoid forms of Campylobacter jejuni ATCC 29428. J Appl Bacteriol 60: 103-110.
78. Moran AP & Upton ME (1987) Factors affecting production of coccoid forms by Campylobacter jejuni on solid media during incubation. J Appl Bacteriol 62: 527-537.
79. Moskovitz J (2005) Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochim Biophys Acta 1703: 213-219.
80. Murphy C, Carroll C & Jordan KN (2006) Environmental survival mechanisms of the foodborne pathogen Campylobacter jejuni. J Appl Microbiol 100: 623-632.
81. Nachamkin I, Allos BM & Ho T (1998) Campylobacter species and Guillain-Barre syndrome. Clin Microbiol Rev 11: 555-567.
82. Nichols GL, Richardson JF, Sheppard SK, Lane C & Sarran C (2012) Campylobacter epidemiology: a descriptive study reviewing 1 million cases in England and Wales between 1989 and 2011. BMJ Open 2: e001179.
83. Nielsen EM, Engberg J, Fussing V, Petersen L, Brogren CH & On SL (2000) Evaluation of phenotypic and genotypic methods for subtyping Campylobacter jejuni isolates from humans, poultry, and cattle. J Clin Microbiol 38: 3800-3810.
84. Ogden ID, MacRae M, Johnston M, Strachan NJ, Cody AJ, Dingle KE & Newell DG (2007) Use of multilocus sequence typing to investigate the association between the presence of Campylobacter spp. in broiler drinking water and Campylobacter colonization in broilers. Appl Environ Microbiol 73: 5125-5129.
85. On SLW, Dorrell N, Petersen L, Bang DD, Morris S, Forsythe SJ & Wren BW (2006) Numerical analysis of DNA microarray data of Campylobacter jejuni strains correlated with survival, cytolethal distending toxin and haemolysin analyses. Int J Med Microbiol 296: 353-363.
86. O'Reilly CE, Bowen AB, Perez NE et al. (2007) A waterborne outbreak of gastroenteritis with multiple etiologies among resort island visitors and residents: Ohio, 2004. Clin Infect Dis 44: 506-512.
87. Palyada K, Threadgill D & Stintzi A (2004) Iron acquisition and regulation in Campylobacter jejuni. J Bacteriol 186: 4714-4729.
88. 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.
89. Parkhill J, Wren BW, Mungall K et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668.
90. Patrone V, Campana R, Vallorani L, Dominici S, Federici S, Casadei L, Gioacchini AM, Stocchi V & Baffone W (2013) CadF expression in Campylobacter jejuni strains incubated under low-temperature water microcosm conditions which induce the viable but non-culturable (VBNC) state. Antonie Van Leeuwenhoek 103: 979-988.
91. Pearson AD, Greenwood M, Healing TD, Rollins D, Shahamat M, Donaldson J & Colwell RR (1993) Colonization of broiler chickens by waterborne Campylobacter jejuni. Appl Environ Microbiol 59: 987-996.
92. Pearson BM, Pin C, Wright J, I'Anson K, Humphrey T & Wells JM (2003) Comparative genome analysis of Campylobacter jejuni using whole genome DNA microarrays. FEBS Lett 554: 224-230.
93. Perez-Boto D, Garcia-Pena FJ, Abad-Moreno JC, Hurtado-Pizarro MD, Perez-Cobo I & Echeita MA (2010) Drinking water as the source of Campylobacter coli infection in grandparent heavy breeders. Avian Pathol 39: 483-487.
94. Pesci EC, Cottle DL & Pickett CL (1994) Genetic, enzymatic, and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni. Infect Immun 62: 2687-2694.
95. Pickett CL, Auffenberg T, Pesci EC, Sheen VL & Jusuf SS (1992) Iron acquisition and hemolysin production by Campylobacter jejuni. Infect Immun 60: 3872-3877.
96. Plummer PJ (2012) LuxS and quorum-sensing in Campylobacter. Front Cell Infect Microbiol 2: 22.
97. Poole LB, Godzik A, Nayeem A & Schmitt JD (2000) AhpF can be dissected into two functional units: tandem repeats of two thioredoxin-like folds in the N-terminus mediate electron transfer from the thioredoxin reductase-like C-terminus to AhpC. Biochemistry 39: 6602-6615.
98. Purdy D, Cawthraw S, Dickinson JH, Newell DG & Park SF (1999) Generation of a superoxide dismutase (SOD)-deficient mutant of Campylobacter coli: evidence for the significance of SOD in Campylobacter survival and colonization. Appl Environ Microbiol 65: 2540-2546.
99. Rainey PB, Hansen SK, Haagensen JAJ & Molin S (2007) Evolution of species interactions in a biofilm community. Nature 445: 533-536.
100. Rasmussen JJ, Vegge CS, Frokiaer H, Howlett RM, Krogfelt KA, Kelly DJ & Ingmer H (2013) Campylobacter jejuni carbon starvation protein A (CstA) is involved in peptide utilization, motility and agglutination, and has a role in stimulation of dendritic cells. J Med Microbiol 62: 1135-1143.
101. Reeser RJ, Medler RT, Billington SJ, Jost BH & Joens LA (2007) Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl Environ Microbiol 73: 1908-1913.
102. Reuter M, Mallett A, Pearson BM & van Vliet AHM (2010) Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl Environ Microbiol 76: 2122-2128.
103. Rollins DM & Colwell RR (1986) Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Appl Environ Microbiol 52: 531-538.
104. Saha SK, Saha S & Sanyal SC (1991) Recovery of injured Campylobacter jejuni cells after animal passage. Appl Environ Microbiol 57: 3388-3389.
105. Sails AD, Swaminathan B & Fields PI (2003) Clonal complexes of Campylobacter jejuni identified by multilocus sequence typing correlate with strain associations identified by multilocus enzyme electrophoresis. J Clin Microbiol 41: 4058-4067.
106. Sampathkumar B, Napper S, Carrillo CD, Willson P, Taboada E, Nash JH, Potter AA, Babiuk LA & Allan BJ (2006) Transcriptional and translational expression patterns associated with immobilized growth of Campylobacter jejuni. Microbiology 152: 567-577.
107. Sanders SQ, Boothe DH, Frank JF & Arnold JW (2007) Culture and detection of Campylobacter jejuni within mixed microbial populations of biofilms on stainless steel. J Food Prot 70: 1379-1385.
108. Sasahara KC & Zottola EA (1993) Biofilm formation by Listeria monocytogenes utilizes a primary colonizing microorganism in flowing systems. J Food Protect 56: 1022-1028.
109. Schallenberg M, Bremer PJ, Henkel S, Launhardt A & Burns CW (2005) Survival of Campylobacter jejuni in water: effect of grazing by the freshwater crustacean Daphnia carinata (Cladocera). Appl Environ Microbiol 71: 5085-5088.
110. Sheppard SK, Dallas JF, Strachan NJ et al. (2009) Campylobacter genotyping to determine the source of human infection. Clin Infect Dis 48: 1072-1078.
111. Sheppard SK, Didelot X, Meric G, Torralbo A, Jolley KA, Kelly DJ, Bentley SD, Maiden MC, Parkhill J & Falush D (2013) Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. P Natl Acad Sci USA 110: 11923-11927.
112. Snelling WJ, Moore JE, McKenna JP, Lecky DM & Dooley JS (2006) Bacterial-protozoa interactions; an update on the role these phenomena play towards human illness. Microbes Infect 8: 578-587.
113. Sopwith W, Birtles A, Matthews M, Fox A, Gee S, Painter M, Regan M, Syed Q & Bolton E (2008) Identification of potential environmentally adapted Campylobacter jejuni strain, United Kingdom. Emerg Infect Dis 14: 1769-1773.
114. Spencer SEF, Marshall J, Pirie R, Campbell D, Baker MG & French NP (2012) The spatial and temporal determinants of campylobacteriosis notifications in New Zealand, 2001-2007. Epidemiol Infect 140: 1663-1677.
115. Stabler RA, Larsson JT, Al-Jaberi S et al. (2013) Characterization of water and wildlife strains as a subgroup of Campylobacter jejuni using DNA microarrays. Environ Microbiol 15: 2371-2383.
116. Stintzi A, van Vliet AH & Ketley JM (2008) Iron metabolism, transport, and regulation. Campylobacter 3rd edn, (Nachamkin I, Szymanski CM & Blaser MJ, eds), pp. 591-610. American Society for Microbiology Press, Washington DC.
117. Strachan NJ, Gormley FJ, Rotariu O et al. (2009) Attribution of Campylobacter infections in northeast Scotland to specific sources by use of multilocus sequence typing. J Infect Dis 199: 1205-1208.
118. Svensson SL, Davis LM, MacKichan JK, Allan BJ, Pajaniappan M, Thompson SA & Gaynor EC (2009) The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol Microbiol 71: 253-272.
119. Taboada EN, Acedillo RR, Carrillo CD, Findlay WA, Medeiros DT, Mykytczuk OL, Roberts MJ, Valencia CA, Farber JM & Nash JH (2004) Large-scale comparative genomics meta-analysis of Campylobacter jejuni isolates reveals low level of genome plasticity. J Clin Microbiol 42: 4566-4576.
120. Taboada EN, Mackinnon JM, Luebbert CC, Gannon VP, Nash JH & Rahn K (2008) Comparative genomic assessment of Multi-Locus Sequence Typing: rapid accumulation of genomic heterogeneity among clonal isolates of Campylobacter jejuni. BMC Evol Biol 8: 229.
121. Talibart R, Denis M, Castillo A, Cappelier JM & Ermel G (2000) Survival and recovery of viable but noncultivable forms of Campylobacter in aqueous microcosm. Int J Food Microbiol 55: 263-267.
122. Tam CC, Rodrigues LC, Viviani L et al. (2012) Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut 61: 69-77.
123. Taylor EV, Herman KM, Ailes EC, Fitzgerald C, Yoder JS, Mahon BE & Tauxe RV (2013) Common source outbreaks of Campylobacter infection in the USA, 1997-2008. Epidemiol Infect 141: 987-996.
124. Teh KH, Flint S & French N (2010) Biofilm formation by Campylobacter jejuni in controlled mixed-microbial populations. Int J Food Microbiol 143: 118-124.
125. Tholozan JL, Cappelier JM, Tissier JP, Delattre G & Federighi M (1999) Physiological characterization of viable-but-nonculturable Campylobacter jejuni cells. Appl Environ Microbiol 65: 1110-1116.
126. Trachoo N, Frank JF & Stern NJ (2002) Survival of Campylobacter jejuni in biofilms isolated from chicken houses. J Food Prot 65: 1110-1116.
127. Uhlmann S, Galanis E, Takaro T, Mak S, Gustafson L, Embree G, Bellack N, Corbett K & Isaac-Renton J (2009) Where's the pump? Associating sporadic enteric disease with drinking water using a geographic information system, in British Columbia, Canada, 1996-2005. J Water Health 7: 692-698.
128. 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.
129. Wassenaar TM & Newell DG (2000) Genotyping of Campylobacter spp. Appl Environ Microbiol 66: 1-9.
130. Wells DH & Long SR (2002) The Sinorhizobium meliloti stringent response affects multiple aspects of symbiosis. Mol Microbiol 43: 1115-1127.
131. Williams NJ, Jones TR, Leatherbarrow HJ, Birtles RJ, Lahuerta-Marin A, Bennett M & Winstanley C (2010) Isolation of a novel Campylobacter jejuni clone associated with the bank vole, Myodes glareolus. Appl Environ Microbiol 76: 7318-7321.
132. Wilson DJ, Gabriel E, Leatherbarrow AJ, Cheesbrough J, Gee S, Bolton E, Fox A, Fearnhead P, Hart CA & Diggle PJ (2008) Tracing the source of campylobacteriosis. PLoS Genet 4: e1000203.
133. Xavier JB & Foster KR (2007) Cooperation and conflict in microbial biofilms. P Natl Acad Sci USA 104: 876-881.
134. Ziprin RL & Harvey RB (2004) Inability of cecal microflora to promote reversion of viable nonculturable Campylobacter jejuni. Avian Dis 48: 647-650.
135. Ziprin RL, Droleskey RE, Hume ME & Harvey RB (2003) Failure of viable nonculturable Campylobacter jejuni to colonize the cecum of newly hatched leghorn chicks. Avian Dis 47: 753-758.