Advertisement

Antonie van Leeuwenhoek

, Volume 96, Issue 4, pp 377–394 | Cite as

Survival mechanisms and culturability of Campylobacter jejuni under stress conditions

  • D. Nathan Jackson
  • Bailey Davis
  • Sandra M. Tirado
  • Megha Duggal
  • Jessica K. van Frankenhuyzen
  • Deanna Deaville
  • M. A. K. Wijesinghe
  • Michael Tessaro
  • J. T. Trevors
Review Paper

Abstract

Culture-based isolation and enumeration of bacterial human pathogens from environmental and human food samples has significant limitations. Many pathogens enter a viable but non-culturable (VBNC) state in response to stress, and cannot be detected via culturing methods. Favourable growth conditions with a source of energy and an ideal stoichiometric ratio of carbon to inorganic elements can reverse this VBNC state. This review will focus on the bacterium Campylobacter jejuni which is a leading cause of food borne illness in the developed world. C. jejuni can enter a VBNC state in response to extremes in: pH, moisture content, temperature, nutrient content and salinity. Once in a VBNC state, the organism must maintain an energy balance from substrate oxidation through respiration to grow, divide and remain viable. The goal of this review is a greater understanding of how abiotic stress and thermodynamics influence the viability of C. jejuni.

Keywords

Campylobacter jejuni VBNC Abiotic stress Bacterial thermodynamics Cell division Environment Gene expression Foodborne illness Growth Nutrient stress Phase changes Survival 

References

  1. Abram DD, Potter NN (1984) Survival of Campylobacter jejuni at different temperatures in broth, beef, chicken and cod supplemented with sodium chloride. J Food Prot 47(10):795–800Google Scholar
  2. Allos BM (2001) Campylobacter jejuni Infections: update on emerging issues and trends. Clin Infect Dis 32(8):1201–1206PubMedCrossRefGoogle Scholar
  3. Alter T, Scherer K (2006) Stress response of Campylobacter spp. and its role in food processing. J Vet Med B Infect Dis Vet Public Health 53(8):351–357PubMedGoogle Scholar
  4. 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(1):83–91PubMedCrossRefGoogle Scholar
  5. 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(16):4798–4804PubMedGoogle Scholar
  6. Barer MR, Harwood CR (1999) Bacterial viability and culturability. Adv Microb Physiol 41:93–137PubMedCrossRefGoogle Scholar
  7. Bastolla U, Moya A, Viguera E, van-Ham RCHJ (2004) Genomic determinants of protein folding thermodynamics in prokaryotic organisms. J Mol Biol 343:1451–1466PubMedCrossRefGoogle Scholar
  8. Beard DA, Reed JL, Qian H (2002) Energy balance for analysis of complex metabolic networks. Biophys J 83:79–86PubMedCrossRefGoogle Scholar
  9. Beard DA, Babson E, Curtis E, Qian H (2004) Thermodynamic constraints for biochemical networks. J Theor Biol 228:327–333PubMedCrossRefGoogle Scholar
  10. Beery JT, Hugdahl MB, Doyle MP (1988) Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl Environ Microbiol 54(10):2365–2370PubMedGoogle Scholar
  11. Beumer RR, Devries J, Rombouts FM (1992) Campylobacter jejuni nonculturable coccoid cells. Int J Food Microbiol 15(1–2):153–163PubMedCrossRefGoogle Scholar
  12. Blaser MJ, Hardesty HL, Powers B, Wang WL (1980) Survival of Campylobacter fetus subsp. jejuni in biological milieus. J Clin Microbiol 11(4):309–313PubMedGoogle Scholar
  13. Bolton FJ, Coates D (1983) A study of the oxygen and carbon dioxide requirements of thermophilic Campylobacters. J Clin Pathol 36(7):829–834PubMedCrossRefGoogle Scholar
  14. Bolton FJ, Hinchliffe PM, Coates D, Robertson L (1982) A most probable number method for estimating small numbers of Campylobacters in water. J Hyg 89(2):185–190Google Scholar
  15. Boucher SN, Slater ER, Chamberlain AH, Adams MR (1994) Production and viability of coccoid forms of Campylobacter jejuni. J Appl Bacteriol 77(3):303–307PubMedGoogle Scholar
  16. Bowman C, Flint J, Pollari F (2003) Canadian integrated surveillance report: Salmonella, Campylobacter, pathogenic E. coli and Shigella, from 1996 to 1999. Can Commun Dis Rep 29S(1):1–39Google Scholar
  17. Boysen L, Knochel S, Rosenquist H (2007) Survival of Campylobacter jejuni in different gas mixtures. FEMS Microbiol Lett 266(2):152–157PubMedCrossRefGoogle Scholar
  18. Bras AM, Chatterjee S, Wren BW, Newell DG, Ketley JM (1999) A novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J Bacteriol 181(10):3298–3302PubMedGoogle Scholar
  19. 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(2):733–741PubMedGoogle Scholar
  20. Candon HL, Allan BJ, Fraley CD, Gaynor EC (2007) Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J Bacteriol 189(22):8099–8108PubMedCrossRefGoogle Scholar
  21. Cappelier JM, Lazaro B, Rossero A, Fernandez-Astorga A, Federighi M (1997) Double staining (CTC-DAPI) for detection and enumeration of viable but non-culturable Campylobacter jejuni cells. Vet Res 28(6):547–555PubMedGoogle Scholar
  22. Cappelier JM, Magras C, Jouve JL, Federighi M (1999) Recovery of viable but non-culturable Campylobacter jejuni cells in two animal models. Food Microbiol 16(4):375–383CrossRefGoogle Scholar
  23. Carlon E, Heim T (2006) Thermodynamics of RNA/DNA hybridization in high-density oligonucleotide microarrays. Physica A 362:433–449CrossRefGoogle Scholar
  24. Chaveerach P, ter Huurne AAHM, Lipman LJA, van Knapen F (2003) Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl Environ Microbiol 69(1):711–714PubMedCrossRefGoogle Scholar
  25. Chen G, Strevett KA (2003) Impact of carbon and nitrogen conditions on E.coli surface thermodynamics. Colloid Surf 28:135–146CrossRefGoogle Scholar
  26. Churruca E, Girbau C, Martínez I, Mateo E, Alonso R, Fernandez-Astorga A (2007) Detection of Campylobacter jejuni and Campylobacter coli in chicken meat samples by real-time nucleic acid sequence-based amplification with molecular beacons. Int J Food Microbiol 117(1):85–90PubMedCrossRefGoogle Scholar
  27. Colwell RR, Huq A (1994) Environmental reservoir of Vibrio cholerae. The causative agent of cholera. Ann NY Acad Sci 740:44–54PubMedCrossRefGoogle Scholar
  28. 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(5):886–892PubMedCrossRefGoogle Scholar
  29. Cools I, D’Haese E, Uyttendaele M, Storms E, Nelis HJ, Debevere J (2005) Solid phase cytometry as a tool to detect viable but non-culturable cells of Campylobacter jejuni. J Microbiol Methods 63(2):107–114PubMedCrossRefGoogle Scholar
  30. Doyle MP, Roman DJ (1982) Response of Campylobacter jejuni to sodium chloride. Appl Environ Microbiol 43(3):561–565PubMedGoogle Scholar
  31. Farber JM (1991) Microbiological aspects of modified-atmosphere packaging technology: a review. J Food Prot 54(1):58–70Google Scholar
  32. Federighi M, Tholozan JL, Cappelier JM, Tissier JP, Jouve JL (1998) Evidence of non-coccoid viable but non-culturable Campylobacter jejuni cells in microcosm water by direct viable count, CTC-DAPI double staining, and scanning electron microscopy. Food Microbial 15(5):539–550CrossRefGoogle Scholar
  33. Friedman CR, Neimann J, Wegener HC, Tauxe RV (2000) Epidemiology of Campylobacter jejuni in the United States and other industrialized nations. In: Nachamkin I, Blaser MJ (eds) Campylobacter. ASM Press, Washington, pp 121–138Google Scholar
  34. Fullerton KE, Ingram LA, Jones TF, Anderson BJ, McCarthy PV, Hurd S, Shiferaw B, Vugia D, Haubert N, Hayes T, Wedel S, Scallan E, Henao O, Angulo FJ (2007) Sporadic Campylobacter infection in infants: a population-based surveillance case–control study. Pediatr Infect Dis J 26(1):19–24PubMedCrossRefGoogle Scholar
  35. Garenaux A, Jugiau F, Rama F, de Jonge R, Denis M, Federighi M, Ritz M (2008) Survival of Campylobacter jejuni strains from different origins under oxidative stress conditions: effect of temperature. Curr Microbiol 56(4):293–297PubMedCrossRefGoogle Scholar
  36. Gaynor EC, Cawthraw S, Manning G, MacKichan JK, Falkow S, Newell DG (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(2):503–517PubMedCrossRefGoogle Scholar
  37. 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(1):8–27PubMedCrossRefGoogle Scholar
  38. Gilbert C, Hanning I, Vaughn B, Kanta H, Slavik M (2007) Comparison of cytolethal distending toxin and invasion abilities in Campylobacter jejuni isolated from clinical patients and poultry. J Food Safety 29(1):73–82CrossRefGoogle Scholar
  39. Gould GW (1995) New methods of food preservation. Blackie Academic & Professional, London, p 324Google Scholar
  40. Guccione E, Leon-Kempis MDR, Pearson BM, Hitchin E, Mulholland F, van Dieman 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(1):77–93PubMedCrossRefGoogle Scholar
  41. Guerry P (2007) Campylobacter flagella: not just for motility. Trends Microbiol 15(10):456–461PubMedCrossRefGoogle Scholar
  42. Guerry P, Szymanski CM (2008) Campylobacter sugars sticking out. Trends Microbiol 16(9):428–435PubMedCrossRefGoogle Scholar
  43. Hanninen ML, Haajanen H, Pummi T, Wermundsen K, Katila ML, Sarkkinen H, Miettinen I, Rautelin H (2003) Detection and typing of Campylobacter jejuni and Campylobacter coli and analysis of indicator organisms in three waterborne outbreaks in Finland. Appl Environ Microbiol 69(3):1391–1396PubMedCrossRefGoogle Scholar
  44. Harvey P, Leach S (1998) Analysis of coccal cell formation by Campylobacter jejuni using continuous culture techniques, and the importance of oxidative stress. J Appl Microbiol 85(2):398–404PubMedCrossRefGoogle Scholar
  45. Hazeleger WC, Janse JD, Koenraad PMFJ, 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(7):2713PubMedGoogle Scholar
  46. Hazeleger WC, Wouters JA, Rombouts FM, Abee T (1998) Physiological activity of Campylobacter jejuni far below the minimal growth temperature. Appl Environ Microbiol 64(10):3917PubMedGoogle Scholar
  47. Henry CS, Broadbelt LJ, Hatzimanikatis V (2007) Thermodynamics-based metabolic flux analysis. Biophys J 92:1792–1805PubMedCrossRefGoogle Scholar
  48. Hofreuter D, Novik V, Galan JE (2008) Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell Host Microbe 4(5):425–433PubMedCrossRefGoogle Scholar
  49. Holler C, Martin W (1998) Evaluation of the direct viable count method for temperature stressed Campylobacter coli. J Microbiol Methods 33(2):157–162CrossRefGoogle Scholar
  50. Hughes NJ, Clayton CL, Chalk PA, Kelly DJ (1998) Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate:flavodoxin and 2-oxoglutarate:acceptor oxidoreductases which mediate electron transport to NADP. J Bacteriol 180(5):1119–1128PubMedGoogle Scholar
  51. Inglis GD, Kalischuk LD (2003) Use of PCR for direct detection of Campylobacter species in bovine feces. Appl Environ Microbiol 69(6):3435–3447PubMedCrossRefGoogle Scholar
  52. Inoue D, Tsutsui H, Yamazaki Y, Sei K, Soda S, Fujita M, Ike M (2008) Application of real-time polymerase chain reaction (PCR) coupled with ethidium monoazide treatment for selective quantification of viable bacteria in aquatic environment. Water Sci Technol 58(5):1107–1112PubMedCrossRefGoogle Scholar
  53. IUPAC (1997) Compendium of chemical terminology, 2nd edn. (the “Gold Book”). Compiled by McNaught AD, Wilkinson A. Blackwell Scientific Publications, OxfordGoogle Scholar
  54. Jones DM, Curry A, Sutcliffe EM (1991a) Ultrastructure of coccal forms of Campylobacter jejuni—are these viable but non-culturable. J Med Microbiol 34(4):VI–VIIGoogle Scholar
  55. Jones DM, Sutcliffe EM, Curry A (1991b) Recovery of viable but non-culturable Campylobacter jejuni. J Gen Microbiol 137(10):2477–2482PubMedGoogle Scholar
  56. Joshua GWP, Guthrie-Irons C, Karlyshev AV, Wren BW (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152(2):387–396PubMedCrossRefGoogle Scholar
  57. Katzav M, Isohanni P, Lund M, Hakkinen M, Lyhs U (2008) PCR assay for the detection of Campylobacter in marinated and non-marinated poultry products. Food Microbiol 25(7):908–914PubMedCrossRefGoogle Scholar
  58. Kelana LC, Griffiths MW (2003a) Use of an autobioluminescent Campylobacter jejuni to monitor cell survival as a function of temperature, pH, and sodium chloride. J Food Prot 66(11):2032–2037PubMedGoogle Scholar
  59. Kelana LC, Griffiths MW (2003b) Growth of autobioluminescent Campylobacter jejuni in response to various environmental conditions. J Food Prot 66(11):1190–1197PubMedGoogle Scholar
  60. Kell DB, Kapreylants AS, Weichart DH, Harwood CL, Barer MR (1998) Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Ant van Leeuvenhoek 73(2):169–187CrossRefGoogle Scholar
  61. Kelly DJ (2001) The physiology and metabolism of Campylobacter jejuni and Helicobacter pylori. J Appl Microbiol 90(S6):16S–24SCrossRefGoogle Scholar
  62. Kelly AF, Park S, Bovill R, Mackey BM (2001) Survival of Campylobacter jejuni during stationary phase: evidence for the absence of a phenotypic stationary-phase response. Appl Environ Microbiol 67(5):2248–2254PubMedCrossRefGoogle Scholar
  63. Konkel ME, Kim BJ, Klena JB, Young CR, Ziprin R (1998) Characterization of the thermal stress response of Campylobacter jejuni. Infect Immun 66(8):3666PubMedGoogle Scholar
  64. Korhonen LK, Martikainen PJ (1991) Comparison of the survival of Campylobacter jejuni and Campylobacter coli in culturable form in surface water. Can J Microbiol 37(7):530–533PubMedGoogle Scholar
  65. Larazo 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(10):4677–4681Google Scholar
  66. Leach S, Harvey P, Wait 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(5):631–640PubMedGoogle Scholar
  67. Levin RE (2007) Campylobacter jejuni: a review of its characteristics, pathogenicity, ecology, distribution, subspecies characterization and molecular methods of detection. Food Biotechnol 21(3–4):271–347CrossRefGoogle Scholar
  68. Lin S, Wang X, Zheng H, Mao Z, Sun Y, Jiang B (2008) Direct detection of Campylobacter jejuni in human stool samples by real-time PCR. Can J Microbiol 54(9):742–747PubMedCrossRefGoogle Scholar
  69. Ma Y, Hanning I, Slavik M (2009) Stress-induced adaptive tolerance response and virulence gene expression in Campylobacter jejuni. J Food Safety 29(1):126–143CrossRefGoogle Scholar
  70. Martin JD, Werner BG, Hotchkiss JH (2003) Effects of carbon dioxide on bacterial growth parameters in milk as measured by conductivity. J Dairy Sci 86(6):1932–1940PubMedCrossRefGoogle Scholar
  71. Martinez-Rodriguez A, Kelly AF, Park SF, Mackey BM (2004) Emergence of variants with altered survival properties in stationary phase cultures of Campylobacter jejuni. Int J Food Microbiol 90(3):321–329PubMedCrossRefGoogle Scholar
  72. Mateo E, Carcamo J, Urquijo M, Perales I, Fernandez-Astorga A (2005) Evaluation of a PCR assay for the detection and identification of Campylobacter jejuni and Campylobacter coli in retail poultry products. Res Microbiol 156(4):568–574PubMedCrossRefGoogle Scholar
  73. Mavrovouniotis ML (1991) Estimation of standard Gibbs energy changes of biotransformation. Biol Chem 266(22):14440–14445Google Scholar
  74. McCarty PL (1975) Stoichiometry of biological reactions. Progr Water Technol 7:157–172Google Scholar
  75. Medeiros D, Hofmann L (2002) Isolation of thermophilic campylobacter from food. Report MFLP-46, Health CanadaGoogle Scholar
  76. 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(6):512–516PubMedGoogle Scholar
  77. Merino FJ, Agulla A, Villasante PA, Diaz A, Saz JV, Velasco AC (1986) Comparative efficacy of seven selective media for isolating Campylobacter jejuni. J Clin Microbiol 24(3):451–452PubMedGoogle Scholar
  78. Mihaljevic RR, Sikic M, Klancnik A, Brumini G, Mozina SS, Abram M (2007) Environmental stress factors affecting survival and virulence of Campylobacter jejuni. Microb Pathog 43(2–3):120–125PubMedCrossRefGoogle Scholar
  79. Miller RA, Britigan BE (1997) Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10(1):1–18PubMedGoogle Scholar
  80. Moen B, Oust A, Langsrud O, Dorrell N, Marsden GL, Hinds J, Kohler A, Wren BW, Rudi K (2005) Explorative multifactor approach for investigating global survival mechanisms of Campylobacter jejuni under environmental conditions. Appl Environ Microbiol 71(4):2086–2094PubMedCrossRefGoogle Scholar
  81. Murphy C, Carroll C, Jordan KN (2003a) Identification of a novel stress resistance mechanism in Campylobacter jejuni. J Appl Microbiol 95(4):704–708PubMedCrossRefGoogle Scholar
  82. Murphy C, Carroll C, Jordan KN (2003b) Induction of an adaptive tolerance response in the foodborne pathogen Campylobacter jejuni. FEMS Microbiol Lett 223(1):89–93PubMedCrossRefGoogle Scholar
  83. Murphy C, Carroll C, Jordan KN (2006) Environmental survival mechanisms of the foodborne pathogen Campylobacter jejuni. J Appl Microbiol 100:623–632PubMedCrossRefGoogle Scholar
  84. Oliver JD (1993) Formation of viable but nonculturable cells. Starvation in bacteria. Plenum, NY, pp 239–272Google Scholar
  85. Oliver JD (2005) The viable but nonculturable state in bacteria. J Microbiol 43:93–100PubMedGoogle Scholar
  86. Otwell WS, Kristinsson HG, Balaban MO (2006) Modified atmospheric processing and packaging of fish: filtered smokes, carbon monoxide, and reduced oxygen packaging. Blackwell, Ames, p 243Google Scholar
  87. Park SF (2002) The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int J Food Microbiol 74(3):177–188PubMedCrossRefGoogle Scholar
  88. Park SF (2005) Campylobacter jejuni stress responses during survival in the food chain and colonization. In: Ketley JM, Konkel ME (eds) Campylobacter molecular and cellular biology. Horizon Bioscience, Wymondham, pp 311–330Google Scholar
  89. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, Chillingworth T, Davies RM, Feltwell T, Holroyd S, Jagels K, Karlyshev AV, Moule S, Pallen MJ, Penn CW, Quail MA, Rajandream MA, Rutherford KM, van Vliet AH, Whitehead S, Barrell BG (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403(6770):665–668PubMedCrossRefGoogle Scholar
  90. Phillips CA (1996) Review: modified atmosphere packaging and its effects on the microbiological quality and safety. Int J Food Sci Tech 31(6):463CrossRefGoogle Scholar
  91. Pickert A, Botzenhart K (1985) Survival of Campylobacter jejuni in drinking water, river water and sewage. Zentralbl Bakteriol Mikrobiol Hyg [B] 182(1):49–57Google Scholar
  92. Qian H, Beard DA, Liang SD (2003) Stoichiometric network theory for nonequilibrium biochemical systems. Eur J Biochem 270:415–421PubMedCrossRefGoogle Scholar
  93. Reezal A, McNeil B, Anderson JG (1998) Effect of low-osmolality nutrient media on growth and culturability of Campylobacter species. Appl Environ Microbiol 64(12):4643–4649PubMedGoogle Scholar
  94. Reid AN, Pandey R, Palyada K, Naikare H, Stintzi A (2008) Identification of Campylobacter jejuni genes involved in the response to acidic pH and stomach transit. Appl Environ Microbiol 74(5):1583–1597PubMedCrossRefGoogle Scholar
  95. 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(3):531–538PubMedGoogle Scholar
  96. Rowan NJ (2004) Viable but non-culturable forms of food and waterborne bacteria: quo vadis? Trends Food Sci Technol 15(9):462–467CrossRefGoogle Scholar
  97. Rudi K, Moen B, Dromtorp SM, Holck AL (2005) Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Appl Environ Microbiol 71(2):1018–1024PubMedCrossRefGoogle Scholar
  98. Ruoff P, Zakhartsev M, Westerhoff HV (2007) Temperature compensation through systems biology. FEBS J 274:940–950PubMedCrossRefGoogle Scholar
  99. Saha SK, Saha S, Sanyal SC (1991) Recovery of injured Campylobacter jejuni cells after animal passage. Appl Environ Microbiol 57:3388–3389PubMedGoogle Scholar
  100. Sails AD, Fox AJ, Bolton FJ, Wareing DRA, Greenway DLA (2003) A real-time PCR assay for the detection of Campylobacter jejuni in foods after enrichment culture. Appl Environ Microbiol 69(3):1383–1390PubMedCrossRefGoogle Scholar
  101. Scherer K, Bartelt E, Sommerfeld C, Hildebrandt G (2006) Comparison of different sampling techniques and enumeration methods for the isolation and quantification of Campylobacter spp. in raw retail chicken legs. Int J Food Microbiol 108(1):115–119PubMedCrossRefGoogle Scholar
  102. Schmidt H, Hensel M (2004) Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17(1):14–56PubMedCrossRefGoogle Scholar
  103. Sellars MJ, Hall SJ, Kelly DJ (2002) Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J Bacteriol 184(15):4187–4196PubMedCrossRefGoogle Scholar
  104. Sleator RD, Wouters J, Gahan CGM, Abee T, Hill C (2001) Analysis of the role of opuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes. Appl Environ Microbiol 67(6):2692–2698PubMedCrossRefGoogle Scholar
  105. Solow BT, Cloak OM, Fratamico PM (2003) Effect of temperature on viability of Campylobacter jejuni and Campylobacter coli on raw chicken or pork skin. J Food Prot 66(11):2023–2031PubMedGoogle Scholar
  106. Stephens PJ, Druggan P, Caron GN (2000) Stressed Salmonella are exposed to reactive oxygen species from two independent sources during recovery in conventional culture media. Int J Food Microbiol 60(2–3):269–285PubMedCrossRefGoogle Scholar
  107. Stintzi A (2003) Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J Bacteriol 185(6):2009–2016PubMedCrossRefGoogle Scholar
  108. Suzuki H, Yamamoto S (2009) Campylobacter contamination in retail poultry meats and by-products in Japan: a literature survey. Food Control 20(6):531–537CrossRefGoogle Scholar
  109. Tangwatcharin P, Chanthachum S, Khopaibool P, Griffiths MW (2006) Morphological and physiological responses of Campylobacter jejuni to stress. J Food Prot 69(11):2747–2753PubMedGoogle Scholar
  110. Tauxe RV, Nachamkin I, Blaser MJ, Tompkins LS (1992) Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. American Society for Microbiology, Washington, pp 121–153Google Scholar
  111. Tenover FC, Patton CM (1987) Naturally occurring auxotrophs of Campylobacter jejuni and Campylobacter coli. J Clin Microbiol 25(9):1659–1661PubMedGoogle Scholar
  112. Tenover FC, Knapp JS, Patton C, Plorde JJ (1985) Use of auxotyping for epidemiological studies of Campylobacter jejuni and Campylobacter coli infections. Infect Immun 48(2):384–388PubMedGoogle Scholar
  113. Terzieva SI, McFeters GA (1991) Survival and injury of Escherichia coli, Campylobacter jejuni, and Yersinia enterocolitica in stream water. Can J Microbiol 37(10):785–790PubMedCrossRefGoogle Scholar
  114. Thies FL, Karch H, Hartung HP, Giegerich G (1999) Cloning and expression of the dnaK gene of Campylobacter jejuni and antigenicity of heat shock protein 70. Infect Immun 67(3):1194–1200PubMedGoogle Scholar
  115. Thomas C, Hill DJ, Mabey M (2002) Culturability injury and morphological dynamics of thermophilic Campylobacter spp. within a laboratory-based aquatic model system. J Appl Microbiol 92(3):433–442PubMedCrossRefGoogle Scholar
  116. Thomas C, Hill DJ, Mabey M (1999) Evaluation of the effect of temperature and nutrients on the survival of Campylobacter spp. in water microcosms. J Appl Microbiol 86:1024–1032PubMedCrossRefGoogle Scholar
  117. Thompson JS, Cahoon FE, Hodge DS (1986) Rate of Campylobacter spp. isolation in three regions of Ontario, Canada, from 1978 to 1985. J Clin Microbiol 24(5):876–878PubMedGoogle Scholar
  118. Torres NV, Voit EO (2002) Target: a useful model. In: Analysis Pathway, Torres NV, Voit EO (eds) Optimization in metabolic engineering. Cambridge University Press, Madrid, pp 1–42Google Scholar
  119. Touati D (2000) Iron and Oxidative stress in bacteria. Arch Biochem Biophys 373:1–6PubMedCrossRefGoogle Scholar
  120. Uyttendaele M, Taverniers I, Debevere J (2001) Effect of sress induced by suboptimal growth factors on survival of Escherichia coli 157:H7. Int J Food Microbiol 66:31–37PubMedCrossRefGoogle Scholar
  121. van Vliet AH, Ketley JM, Park SF, Penn CW (2002) The role of iron in Campylobacter gene regulation, metabolism and oxidative stress defense. FEMS Microbiol Rev 26(2):173–186PubMedCrossRefGoogle Scholar
  122. Velayudhan J, Kelly DJ (2002) Analysis of gluconeogenic and anaplerotic enzymes in Campylobacter jejuni: an essential role for phosphoenolpyruvate carboxykinase. Microbiology 148(3):685–694PubMedGoogle Scholar
  123. 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(1):260–268PubMedCrossRefGoogle Scholar
  124. Verhoeff-Bakkenes L, Hazeleger WC, de Jonge R, Zwietering MH (2009) Campylobacter jejuni: a study on environmental conditions affecting culturability and in vitro adhesion/invasion. J Appl Microbiol 106(3):924–931PubMedCrossRefGoogle Scholar
  125. Wesley RD, Stadelman WJ (1985) The effect of carbon dioxide packaging on detection of Campylobacter jejuni for chicken carcasses. Poult Sci 64(4):763–764PubMedGoogle Scholar
  126. Westfall HN, Rollins DM, Weiss E (1986) Substrate utilization by Campylobacter jejuni and Campylobacter coli Appl Environ Microbiol 52(4):700–705PubMedGoogle Scholar
  127. White D (2000) The physiology and biochemistry of prokaryotes. Oxford University Press Inc, New YorkGoogle Scholar
  128. Williams LK, Jorgensen F, Grogono-Thomas R, Humphrey T (2009) Enrichment culture for the isolation of Campylobacter spp: effects of incubation conditions and the inclusion of blood in selective broths. Int J Food Microbiol 130(2):131–134PubMedCrossRefGoogle Scholar
  129. Wright JA, Grant AJ, Hurd D, Harrison M, Guccione EJ, Kelly DJ, Maskell DJ (2009) Metabolite and transcriptome analysis of Campylobacter jejuni in vitro growth reveals a stationary-phase physiological switch. Microbiology 155(1):80–94PubMedCrossRefGoogle Scholar
  130. 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(3):753–758PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • D. Nathan Jackson
    • 1
  • Bailey Davis
    • 1
  • Sandra M. Tirado
    • 1
  • Megha Duggal
    • 1
  • Jessica K. van Frankenhuyzen
    • 1
  • Deanna Deaville
    • 1
  • M. A. K. Wijesinghe
    • 1
  • Michael Tessaro
    • 2
  • J. T. Trevors
    • 1
  1. 1.School of Environmental SciencesUniversity of GuelphGuelphCanada
  2. 2.Department of Plant AgricultureUniversity of GuelphGuelphCanada

Personalised recommendations