1887

Chapter 32 : Survival Strategies of : Stress Responses, the Viable but Nonculturable State, and Biofilms

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Survival Strategies of : Stress Responses, the Viable but Nonculturable State, and Biofilms, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap32-1.gif /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap32-2.gif

Abstract:

This chapter is divided into three sections. The first covers specific stresses and responses, is organized by the type of stress encountered, and discusses specific gene products or global response pathways that participate in countering the stress condition. The second and third sections cover two different types of pleiotropic whole-population differentiation strategies or outcomes: the viable but nonculturable (VBNC) and coccoid forms of , and biofilms. Also incorporated into the latter two sections are the types of stresses that induce the differentiation, the genes involved in their formation, and the effect of differentiation on survivability or growth of . To date, only two regulatory factors directly affecting heat stress have been characterized, one of which is the RacR (reduced ability to colonize) response regulator. As such, nonculturable cells can be classified as both viable and nonviable, and not necessarily specifically correlated with shape. The majority of research to date on the contribution of biofilms to stress tolerance in has been in the context of survival in aquatic environments. It is important to point out that although this chapter specifically reviewed survival strategies and stress responses, many of the genes and pathways discussed affect multiple or all aspects of the pathogenesis cycle, encompassing colonization, transmission, and virulence.

Citation: Svensson S, Frirdich E, Gaynor E. 2008. Survival Strategies of : Stress Responses, the Viable but Nonculturable State, and Biofilms, p 571-590. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch32

Key Concept Ranking

Two-Component Signal Transduction Systems
0.42877212
0.42877212
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1.
Figure 1.

Biofilms of 81-176 wild-type and isogenic mutants. (A) Static biofilms grown on borosilicate glass were stained with crystal violet and visualized macroscopically (insets) or were processed for scanning electron microscopy (large photographs; bars = 10 μm). The Δ mutant forms more mature biofilms than wild type; conversely, mutants are defective for biofilm formation. In these strains, biofilm levels correlate with levels of a calcofluor white–reactive exopolysaccharide (EPS), which is overproduced in Δ and underproduced in the mutants ( ). (B) Crystal violet–stained biofilms were visualized macroscopically (insets) or by light microscopy (large photographs; magnification, ×10 and ×100). The Δ mutant exhibits an extreme hyperbiofilm phenotype but displays wild-type levels of the CFW-reactive EPS (S. L. Svensson and E. C. Gaynor, unpublished data), suggesting multiple means by which biofilm formation can be upregulated in

Citation: Svensson S, Frirdich E, Gaynor E. 2008. Survival Strategies of : Stress Responses, the Viable but Nonculturable State, and Biofilms, p 571-590. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch32
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555815554.ch32
1. Alonso, J. L.,, S. Mascellaro,, Y. Moreno,, M. A. Ferrus, and, J. Hernandez. 2002. Double-staining method for differentiation of morphological changes and membrane integrity of Campylobacter coli cells. Appl. Environ. Microbiol. 68:51515154.
2. Alter, T., and, K. Scherer. 2006. Stress response of Campylobacter spp. and its role in food processing. J. Vet. Med. B Infect. Dis. Vet. Public Health 53:351357.
3. Amano, K., and, Y. Shibata. 1992. Structural studies of peptidoglycans in Campylobacter species. Microbiol. Immunol. 36:961967.
4. Andersen, M. T.,, L. Brondsted,, B. M. Pearson,, F. Mulholland,, M. Parker,, C. Pin,, J. M. Wells, and, H. Ingmer. 2005. Diverse roles for HspR in Campylobacter jejuni revealed by the proteome, transcriptome and phenotypic characterization of an hspR mutant. Microbiology 151:905915.
5. Auld, H.,, D. MacIver, and, J. Klaassen. 2004. Heavy rainfall and waterborne disease outbreaks: the Walkerton example. J. Toxicol. Environ. Health. A 67:18791887.
6. Axelsson-Olsson, D.,, J. Waldenstrom,, T. Broman,, B. Olsen, and, M. Holmberg. 2005. Protozoan Acanthamoeba polyphaga as a potential reservoir for Campylobacter jejuni. Appl. Environ. Microbiol. 71:987992.
7. Baffone, W.,, A. Casaroli,, B. Citterio,, L. Pierfelici,, R. Campana,, E. Vittoria,, E. Guaglianone, and, G. Donelli. 2006. Campylobacter jejuni loss of culturability in aqueous microcosms and ability to resuscitate in a mouse model. Int. J. Food Microbiol. 107:8391.
8. Baillon, M. L.,, A. H. van Vliet,, J. M. Ketley,, C. Constantinidou, and, C. W. Penn. 1999. An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J. Bacteriol. 181:47984804.
9. Balzer, G. J., and, R. J. McLean. 2002. The stringent response genes relA and spoT are important for Escherichia coil biofilms under slow-growth conditions. Can. J. Microbiol. 48:675680.
10. Barer, M. R., and, C. R. Harwood. 1999. Bacterial viability and culturability. Adv. Microb. Physiol. 41:93137.
11. Benaissa, M.,, P. Babin,, N. Quellard,, L. Pezennec,, Y. Cenatiempo, and, J. L. Fauchere. 1996. Changes in Helicobacter pylori ultra-structure and antigens during conversion from the bacillary to the coccoid form. Infect. Immun. 64:23312335.
12. Berry, D.,, C. Xi, and, L. Raskin. 2006. Microbial ecology of drinking water distribution systems. Curr. Opin. Biotechnol. 17:297302.
13. Beumer, R. R.,, J. de Vries, and, F. M. Rombouts. 1992. Campylobacter jejuni non-culturable coccoid cells. Int. J. Food Microbiol. 15:153163.
14. Birk, T.,, H. Ingmer,, M. T. Andersen,, K. Jorgensen, and, L. Brondsted. 2004. Chicken juice, a food-based model system suitable to study survival of Campylobacter jejuni. Lett. Appl. Microbiol. 38:6671.
15. Bode, G.,, P. Malfertheiner,, G. Lehnhardt,, M. Nilius, and, H. Ditschuneit. 1993. Ultrastructural localization of urease of Helicobacter pylori. Med. Microbiol. Immunol. 182:233242.
16. Boucher, S. N.,, E. R. Slater,, A. H. Chamberlain, and, M. R. Adams. 1994. Production and viability of coccoid forms of Campylobacter jejuni. J. Appl. Bacteriol. 77:303307.
17. Branda, S. S.,, S. Vik,, L. Friedman, and, R. Kolter. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13:2026.
18. Bras, A. M.,, S. Chatterjee,, B. W. Wren,, D. G. Newell, and, J. M. Ketley. 1999. A novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J. Bacteriol. 181:32983302.
19. Brondsted, L.,, M. T. Andersen,, M. Parker,, K. Jorgensen, and, H. Ingmer. 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. 71:32053212.
20. Brown, M. R., and, A. Kornberg. 2004. Inorganic polyphosphate in the origin and survival of species. Proc. Natl. Acad. Sci. USA 101:1608516087.
21. Buck, G. E.,, K. A. Parshall, and, C. P. Davis. 1983. Electron microscopy of the coccoid form of Campylobacter jejuni. J. Clin. Microbiol. 18:420421.
22. Buswell, C. M.,, Y. M. Herlihy,, L. M. Lawrence,, J. T. McGuiggan,, P. D. Marsh,, C. W. Keevil, and, S. A. Leach. 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. 64:733741.
23. Butzler, J. P., and, M. B. Skirrow. 1979. Campylobacter enteritis. Clin. Gastroenterol. 8:737765.
24. Cabeen, M. T., and, C. Jacobs-Wagner. 2005. Bacterial cell shape. Nat. Rev. Microbiol. 3:601610.
25. Cabiscol, E.,, J. Tamarit, and, J. Ros. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3:38.
26. Candon, H. L.,, B. J. Allan,, C. D. Fraley, and, E. C. Gaynor. 2007. Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J. Bacteriol. 189:80998108.
27. Cappelier, J. M.,, C. Magras,, J. L. Jouve, and, M. Federighi. 1999a. Recovery of viable but non-culturable Campylobacter jejuni cells in two animal models. Food Microbiol. 16:375383.
28. Cappelier, J. M.,, J. Minet,, C. Magras,, R. R. Colwell, and, M. Federighi. 1999b. Recovery in embryonated eggs of viable but nonculturable Campylobacter jejuni cells and maintenance of ability to adhere to HeLa cells after resuscitation. Appl. Environ. Microbiol. 65:51545157.
29. Cappelier, J. M.,, A. Rossero, and, M. Federighi. 2000. Demonstration of a protein synthesis in starved Campylobacter jejuni cells. Int. J. Food Microbiol. 55:6367.
30. Carrillo, C. D.,, E. Taboada,, J. H. Nash,, P. Lanthier,, J. Kelly,, P. C. Lau,, R. Verhulp,, O. Mykytczuk,, J. Sy,, W. A. Findlay,, K. Amoako,, S. Gomis,, P. Willson,, J. W. Austin,, A. Potter,, L. Babiuk,, B. Allan, and, C. M. Szymanski. 2004. Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J. Biol. Chem. 279:2032720338.
31. Carron, M. A.,, V. R. Tran,, C. Sugawa, and, J. M. Coticchia. 2006. Identification of Helicobacter pylori biofilms in human gastric mucosa. J. Gastrointest. Surg. 10:712817.
32. Champion, O. L.,, M. W. Gaunt,, O. Gundogdu,, A. Elmi,, A. A. Witney,, J. Hinds,, N. Dorrell, and, B. W. Wren. 2005. Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source. Proc. Natl. Acad. Sci. USA 102:1604310648.
33. Chan, K. F.,, H. Le Tran,, R. Y. Kanenaka, and, S. Kathariou. 2001. Survival of clinical and poultry-derived isolates of Campylobacter jejuni at a low temperature (4 degrees C). Appl. Environ. Microbiol. 67:41864191.
34. Chaput, C.,, C. Ecobichon,, N. Cayet,, S. E. Girardin,, C. Werts,, S. Guadagnini,, M. C. Prevost,, D. Mengin-Lecreulx,, A. Labigne, and, I. G. Boneca. 2006. Role of AmiA in the morphological transition of Helicobacter pylori and in immune escape. PLoS Pathog. 2:e97.
35. Chaveerach, P.,, A. A. ter Huurne,, L. J. Lipman, and, F. van Knapen. 2003. Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl. Environ. Microbiol. 69:711714.
36. Chou, S. P.,, R. Dular, and, S. Kasatiya. 1983. Effect of ferrous sulfate, sodium metabisulfite, and sodium pyruvate on survival of Campylobacter jejuni. J. Clin. Microbiol. 18:986987.
37. Clark, C. G.,, L. Price,, R. Ahmed,, D. L. Woodward,, P. L. Melito,, F. G. Rodgers,, F. Jamieson,, B. Ciebin,, A. Li, and, A. Ellis. 2003. Characterization of waterborne outbreak-associated Campylobacter jejuni, Walkerton, Ontario. Emerg. Infect. Dis. 9:12321241.
38. Cools, I.,, M. Uyttendaele,, C. Caro,, E. D’Haese,, H. J. Nelis, and, J. Debevere. 2003. Survival of Campylobacter jejuni strains of different origin in drinking water. J. Appl. Microbiol. 94:886892.
39. Costa, K.,, G. Bacher,, G. Allmaier,, M. G. Dominguez-Bello,, L. Engstrand,, P. Falk,, M. A. de Pedro, and, F. Garcia-del Portillo. 1999. The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J. Bacteriol. 181:37103715.
40. Coticchia, J. M.,, C. Sugawa,, V. R. Tran,, J. Gurrola,, E. Kowalski, and, M. A. Carron. 2006. Presence and density of Helicobacter pylori biofilms in human gastric mucosa in patients with peptic ulcer disease. J Gastrointest. Surg. 10:883889.
41. Day, W. A.,, Jr.,, J. L. Sajecki,, T. M. Pitts, and, L. A. Joens. 2000. Role of catalase in Campylobacter jejuni intracellular survival. Infect. Immun. 68:63376345.
42. Doyle, M. P., and, D. J. Roman. 1981. Growth and survival of Campylobacter fetus subsp. jejuni as a function of temperature and pH. J. Food Prot. 44:596601.
43. Doyle, M. P., and, D. J. Roman. 1982. Response of Campylobacter jejuni to sodium chloride. Appl. Environ. Microbiol. 43:561565.
44. Dykes, G. A.,, B. Sampathkumar, and, D. R. Korber. 2003. Planktonic or biofilm growth affects survival, hydrophobicity and protein expression patterns of a pathogenic Campylobacter jejuni strain. Int. J. Food Microbiol. 89:110.
45. Ehrlich, G. D.,, F. Z. Hu,, K. Shen,, P. Stoodley, and, J. C. Post. 2005. Bacterial plurality as a general mechanism driving persistence in chronic infections. Clin. Orthop. Relat. Res. (473):2024.
46. Elvers, K. T., and, S. F. Park. 2002. Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule. Microbiology 148:14751481.
47. Elvers, K. T.,, S. M. Turner,, L. M. Wainwright,, G. Marsden,, J. Hinds,, J. A. Cole,, R. K. Poole,, C. W. Penn, and, S. F. Park. 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. 57:735750.
48. Elvers, K. T.,, G. Wu,, N. J. Gilberthorpe,, R. K. Poole, and, S. F. Park. 2004. Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli. J. Bacteriol. 186:53325341.
49. Federighi, M.,, J. L. Tholozan,, J. M. Cappelier,, J. P. Tissier, and, J. L. Jouve. 1998. Evidence of non-coccoid viable but nonculturable Campylobacter jejuni cells in microcosm water by direct viable count, CTC-DAPI double staining, and scanning electron microscopy. Food Microbiol. 15:539550.
50. Fox, E. M.,, M. Raftery,, A. Goodchild, and, G. L. Mendz. 2007. Campylobacter jejuni response to ox-bile stress. FEMS Immunol. Med. Microbiol. 49:165172.
51. Fredericks, C. E.,, S. Shibata,, S. Aizawa,, S. A. Reimann, and, A. J. Wolfe. 2006. Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay. Mol. Microbiol. 61:734747.
52. Fux, C. A.,, J. W. Costerton,, P. S. Stewart, and, P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:3440.
53. Gaynor, E. C.,, S. Cawthraw,, G. Manning,, J. K. MacKichan,, S. Falkow, and, D. G. Newell. 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. 186:503517.
54. Gaynor, E. C.,, D. H. Wells,, J. K. MacKichan, and, S. Falkow. 2005. The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol. Microbiol. 56:827.
55. Golden, N. J., and, D. W. Acheson. 2002. Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect. Immun. 70:17611771.
56. Grant, K. A., and, S. F. Park. 1995. Molecular characterization of katA from Campylobacter jejuni and generation of a catalase-deficient mutant of Campylobacter coli by interspecific allelic exchange. Microbiology 141(Pt. 6):13691376.
57. Griffiths, P. L. 1993. Morphological changes of Campylobacter jejuni growing in liquid culture. Lett. Appl. Microbiol. 17:152155.
58. Gu, R.,, C. C. Su,, F. Shi,, M. Li,, G. McDermott,, Q. Zhang, and, E. W. Yu. 2007. Crystal structure of the transcriptional regulator CmeR from Campylobacter jejuni. J. Mol. Biol. 372:583593.
59. Guerry, P.,, C. P. Ewing,, M. Schirm,, M. Lorenzo,, J. Kelly,, D. Pattarini,, G. Majam,, P. Thibault, and, S. Logan. 2006. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 60:299311.
60. Hald, B.,, K. Knudsen,, P. Lind, and, M. Madsen. 2001. Study of the infectivity of saline-stored Campylobacter jejuni for day-old chicks. Appl. Environ. Microbiol. 67:23882392.
61. Hazeleger, W.,, C. Arkesteijn,, A. Toorop-Bouma, and, R. Beumer. 1994. Detection of the coccoid form of Campylobacter jejuni in chicken products with the use of the polymerase chain reaction. Int. J. Food Microbiol. 24:273281.
62. Hazeleger, W. C.,, J. D. Janse,, P. M. Koenraad,, R. R. Beumer,, F. M. Rombouts, and, T. Abee. 1995. Temperature-dependent membrane fatty acid and cell physiology changes in coccoid forms of Campylobacter jejuni. Appl. Environ. Microbiol. 61:27132719.
63. Hendrixson, D. R. 2006. A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol. Microbiol. 61:16461659.
64. Hodge, J. P., and, N. R. Krieg. 1994. Oxygen tolerance estimates in Campylobacter species depend on the testing medium. J. Appl. Bacteriol. 77:666673.
65. Holler, C.,, D. Witthuhn, and, B. Janzen-Blunck. 1998. Effect of low temperatures on growth, structure, and metabolism of Campylobacter coli SP10. Appl. Environ. Microbiol. 64:581587.
66. Hudock, J. F.,, A. C. Borger, and, C. W. Kaspar. 2005. Temperature-dependent genome degradation in the coccoid form of Campylobacter jejuni. Curr. Microbiol. 50:110113.
67. Ishikawa, T.,, Y. Mizunoe,, S. Kawabata,, A. Takade,, M. Harada,, S. N. Wai, and, S. Yoshida. 2003. The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni. J. Bacteriol. 185:10101017.
68. Jackson, D. W.,, K. Suzuki,, L. Oakford,, J. W. Simecka,, M. E. Hart, and, T. Romeo. 2002. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184:290301.
69. Jacob, J.,, W. Martin, and, C. Holler. 1993. Characterization of viable but nonculturable stage of C. coli, characterized with respect to electron microscopic findings, whole cell protein and lipooligosaccharide (LOS) patterns. Zentralbl. Mikrobiol. 148:310.
70. Jeon, B.,, K. Itoh,, N. Misawa, and, S. Ryu. 2003. Effects of quorum sensing on flaA transcription and autoagglutination in Campylobacter jejuni. Microbiol. Immunol. 47:833839.
71. Jesudason, M. V.,, D. J. Hentges, and, P. Pongpech. 1989. Colonization of mice by Campylobacter jejuni. Infect. Immun. 57:22792282.
72. Jiang, X., and, T. J. Chai. 1996. Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl. Environ. Microbiol. 62:13001305.
73. Jones, D. M.,, E. M. Sutcliffe, and, A. Curry. 1991. Recovery of viable but non-culturable Campylobacter jejuni. J. Gen. Microbiol. 137:24772482.
74. Jones, D. M.,, E. M. Sutcliffe,, R. Rios,, A. J. Fox, and, A. Curry. 1993. Campylobacter jejuni adapts to aerobic metabolism in the environment. J. Med. Microbiol. 38:145150.
75. Joshua, G. W.,, C. Guthrie-Irons,, A. V. Karlyshev, and, B. W. Wren. 2006. Biofilm formation in Campylobacter jejuni. Microbiology 152:387396.
76. Kalmokoff, M.,, P. Lanthier,, T. L. Tremblay,, M. Foss,, P. C. Lau,, G. Sanders,, J. Austin,, J. Kelly, and, C. M. Szymanski. 2006. Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J. Bacteriol. 188:43124320.
77. Kazwala, R. R.,, J. D. Collins,, J. Hannan,, R. A. Crinion, and, H. O’Mahony. 1990. Factors responsible for the introduction and spread of Campylobacter jejuni infection in commercial poultry production. Vet. Rec. 126:305306.
78. Keevil, C. W. 2003. Rapid detection of biofilms and adherent pathogens using scanning confocal laser microscopy and episcopic differential interference contrast microscopy. Water Sci. Technol. 47:105116.
79. Kelly, A. F.,, S. F. Park,, R. Bovill, and, B. M. Mackey. 2001. Survival of Campylobacter jejuni during stationary phase: evidence for the absence of a phenotypic stationary-phase response. Appl. Environ. Microbiol. 67:22482254.
80. King, C. H.,, E. B. Shotts,, Jr.,, R. E. Wooley, and, K. G. Porter. 1988. Survival of coliforms and bacterial pathogens within protozoa during chlorination. Appl. Environ. Microbiol. 54:30233033.
81. Klancnik, A.,, N. Botteldoorn,, L. Herman, and, S. S. Mozina. 2006. Survival and stress induced expression of groEL and rpoD of Campylobacter jejuni from different growth phases. Int. J. Food Microbiol. 112:2002007.
82. Kogure, K.,, U. Simidu, and, N. Taga. 1979. A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25:415420.
83. Konkel, M. E.,, B. J. Kim,, J. D. Klena,, C. R. Young, and, R. Ziprin. 1998. Characterization of the thermal stress response of Campylobacter jejuni. Infect. Immun. 66:36663672.
84. Kuchma, S. L.,, K. M. Brothers,, J. H. Merritt,, N. T. Liberati,, F. M. Ausubel, and, A. O’Toole, G. 2007. BifA, a c-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189:81658178.
85. Kusters, J. G.,, M. M. Gerrits,, J. A. Van Strijp, and, C. M. Vandenbroucke-Grauls. 1997. Coccoid forms of Helicobacter pylori are the morphologic manifestation of cell death. Infect. Immun. 65:36723679.
86. Lazaro, B.,, J. Carcamo,, A. Audicana,, I. Perales, and, A. Fernandez-Astorga. 1999. Viability and DNA maintenance in nonculturable spiral Campylobacter jejuni cells after long-term exposure to low temperatures. Appl. Environ. Microbiol. 65:46774681.
87. Lehtola, M. J.,, T. Pitkanen,, L. Miebach, and, I. T. Miettinen. 2006. Survival of Campylobacter jejuni in potable water biofilms: a comparative study with different detection methods. Water Sci. Technol. 54:5761.
88. Leon-Kempis Mdel, R.,, E. Guccione,, F. Mulholland,, M. P. Williamson, and, D. J. Kelly. 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. 60:12621275.
89. Lin, J.,, M. Akiba,, O. Sahin, and, Q. Zhang. 2005a. CmeR functions as a transcriptional repressor for the multidrug efflux pump CmeABC in Campylobacter jejuni. Antimicrob. Agents Chemother. 49:10671075.
90. Lin, J.,, C. Cagliero,, B. Guo,, Y. W. Barton,, M. C. Maurel,, S. Payot, and, Q. Zhang. 2005b. Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J. Bacteriol. 187:74177424.
91. Lin, J., and, A. Martinez. 2006. Effect of efflux pump inhibitors on bile resistance and in vivo colonization of Campylobacter jejuni. J. Antimicrob. Chemother. 58:966972.
92. Lin, J.,, L. O. Michel, and, Q. Zhang. 2002. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob. Agents Chemother. 46:21242131.
93. Lin, J.,, O. Sahin,, L. O. Michel, and, Q. Zhang. 2003. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect. Immun. 71:42504259.
94. Macfarlane, S.,, E. Furrie,, G. T. Macfarlane, and, J. F. Dillon. 2007. Microbial colonization of the upper gastrointestinal tract in patients with Barrett’s esophagus. Clin. Infect. Dis. 45:2938.
95. MacKichan, J. K.,, E. C. Gaynor,, C. Chang,, S. Cawthraw,, D. G. Newell,, J. F. Miller, and, S. Falkow. 2004. The Campylobacter jejuni dccRS two-component system is required for optimal in vivo colonization but is dispensable for in vitro growth. Mol. Microbiol. 54:12691286.
96. Martinez-Rodriguez, A.,, A. F. Kelly,, S. F. Park, and, B. M. Mackey. 2004. Emergence of variants with altered survival properties in stationary phase cultures of Campylobacter jejuni. Int. J. Food Microbiol. 90:321329.
97. McCleary, W. R., and, J. B. Stock. 1994. Acetyl phosphate and the activation of two-component response regulators. J. Biol. Chem. 269:3156731572.
98. McCleary, W. R.,, J. B. Stock, and, A. J. Ninfa. 1993. Is acetyl phosphate a global signal in Escherichia coli? J. Bacteriol. 175:27932798.
99. McLennan, M. K.,, D. D. Ringoir,, E. Frirdich,, S. L. Svensson,, D. H. Wells,, H. C. Jarrell,, C. M. Szymanski, and, E. C. Gaynor. 2007. Campylobacter jejuni biofilms up-regulated in the absence of the stringent response utilize a calcofluor white–reactive surface polysaccharide. J. Bacteriol. 190:10971107.
100. Medema, G. J.,, F. M. Schets,, A. W. van de Giessen, and, A. H. Havelaar. 1992. Lack of colonization of 1 day old chicks by viable, non-culturable Campylobacter jejuni. J. Appl. Bacteriol. 72:512516.
101. Mihaljevic, R. R.,, M. Sikic,, A. Klancnik,, G. Brumini,, S. S. Mozina, and, M. Abram. 2007. Environmental stress factors affecting survival and virulence of Campylobacter jejuni. Microb. Pathog. 43:120125.
102. Misawa, N., and, M. J. Blaser. 2000. Detection and characterization of autoagglutination activity by Campylobacter jejuni. Infect. Immun. 68:61686175.
103. Moore, J. E. 2001. Bacterial dormancy in Campylobacter: abstract theory or cause for concern? Int. J. Food Sci. Technol. 36:593600.
104. Moran, A. P., and, M. E. Upton. 1986. A comparative study of the rod and coccoid forms of Campylobacter jejuni ATCC 29428. J. Appl. Bacteriol. 60:103110.
105. Moran, A. P., and, M. E. Upton. 1987. Factors affecting production of coccoid forms by Campylobacter jejuni on solid media during incubation. J. Appl. Bacteriol. 62:527537.
106. Murphy, C.,, C. Carroll, and, K. N. Jordan. 2005. The effect of different media on the survival and induction of stress responses by Campylobacter jejuni. J. Microbiol. Methods 62:161166.
107. Murphy, C.,, C. Carroll, and, K. N. Jordan. 2006. Environmental survival mechanisms of the foodborne pathogen Campylobacter jejuni. J. Appl. Microbiol. 100:623632.
108. Murphy, C.,, C. Carroll, and, K. N. Jordan. 2003a. Identification of a novel stress resistance mechanism in Campylobacter jejuni. J. Appl. Microbiol. 95:704708.
109. Murphy, C.,, C. Carroll, and, K. N. Jordan. 2003b. Induction of an adaptive tolerance response in the foodborne pathogen, Campylobacter jejuni. FEMS Microbiol. Lett. 223:8993.
110. Ng, L. K.,, R. Sherburne,, D. E. Taylor, and, M. E. Stiles. 1985. Morphological forms and viability of Campylobacter species studied by electron microscopy. J. Bacteriol. 164:338343.
111. Nguyen, H. T.,, J. E. Corry, and, C. A. Miles. 2006. Heat resistance and mechanism of heat inactivation in thermophilic campylobacters. Appl. Environ. Microbiol. 72:908913.
112. Nilius, M.,, A. Strohle,, G. Bode, and, P. Malfertheiner. 1993. Coccoid like forms (CLF) of Helicobacter pylori. Enzyme activity and antigenicity. Zentralbl. Bakteriol. 280:259272.
113. Okoli, A. S.,, T. Wadstrom, and, G. L. Mendz. 2007. MiniReview: bioinformatic study of bile responses in Campylobacterales. FEMS Immunol. Med. Microbiol. 49:101123.
114. Oliver, J. D. 2005. The viable but nonculturable state in bacteria. J Microbiol. 43:93100.
115. O’Reilly, C. E.,, A. B. Bowen,, N. E. Perez,, J. P. Sarisky,, C. A. Shepherd,, M. D. Miller,, B. C. Hubbard,, M. Herring,, S. D. Buchanan,, C. C. Fitzgerald,, V. Hill,, M. J. Arrowood,, L. X. Xiao,, R. M. Hoekstra,, E. D. Mintz, and, M. F. Lynch. 2007. A waterborne outbreak of gastroenteritis with multiple etiologies among resort island visitors and residents: Ohio, 2004. Clin. Infect. Dis. 44:506612.
116. O’Toole, G.,, H. B. Kaplan, and, R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:4979.
117. Park, S. F. 2005. Campylobacter jejuni stress responses during survival in the food chain and colonization, p. 311330. In J. M. Ketley and, M. E. Konkel (ed.), Campylobacter: Molecular and Cellular Biology. Horizon Bioscience, Norfolk, United Kingdom.
118. Park, S. F. 2002. The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int. J. Food Microbiol. 74:177188.
119. Parkhill, J.,, B. W. Wren,, K. Mungall,, 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. 403:665668.
120. Parkins, M. D.,, H. Ceri, and, D. G. Storey. 2001. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol. Microbiol. 40:12151226.
121. Patel, R. 2005. Biofilms and antimicrobial resistance. Clin. Orthop. Relat Res. 4147.
122. Pearson, A. D.,, M. Greenwood,, T. D. Healing,, D. Rollins,, M. Shahamat,, J. Donaldson, and, R. R. Colwell. 1993. Colonization of broiler chickens by waterborne Campylobacter jejuni. Appl. Environ. Microbiol. 59:987996.
123. Pesci, E. C.,, D. L. Cottle, and, C. L. Pickett. 1994. Genetic, enzymatic, and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni. Infect. Immun. 62:26872694.
124. Phongsisay, V.,, V. N. Perera, and, B. N. Fry. 2007. Expression of the htrB gene is essential for responsiveness of Salmonella typhimurium and Campylobacter jejuni to harsh environments. Microbiology 153:254262.
125. Pittman, M. S.,, K. T. Elvers,, L. Lee,, M. A. Jones,, R. K. Poole,, S. F. Park, and, D. J. Kelly. 2007. Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol. Microbiol. 63:575590.
126. Purdy, D.,, S. Cawthraw,, J. H. Dickinson,, D. G. Newell, and, S. F. Park. 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. 65:25402546.
127. Purdy, D., and, S. F. Park. 1994. Cloning, nucleotide sequence and characterization of a gene encoding superoxide dismutase from Campylobacter jejuni and Campylobacter coli. Microbiology 140(Pt. 5):12031208.
128. Quinn, T.,, J. M. Bolla,, J. M. Pages, and, S. Fanning. 2007. Antibiotic-resistant Campylobacter: could efflux pump inhibitors control infection? J. Antimicrob. Chemother. 59:12301236.
129. Raetz, C. R., and, C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635700.
130. Raivio, T. L. 2005. Envelope stress responses and gram-negative bacterial pathogenesis. Mol. Microbiol. 56:11191128.
131. Raphael, B. H.,, S. Pereira,, G. A. Flom,, Q. Zhang,, J. M. Ketley, and, M. E. Konkel. 2005. The Campylobacter jejuni response regulator, CbrR, modulates sodium deoxycholate resistance and chicken colonization. J. Bacteriol. 187:36623670.
132. Reeser, R. J.,, R. T. Medler,, S. J. Billington,, B. H. Jost, and, L. A. Joens. 2007. Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl. Environ. Microbiol. 73:19081913.
133. Reezal, A.,, B. McNeil, and, J. G. Anderson. 1998. Effect of low-osmolality nutrient media on growth and culturability of Campylobacter species. Appl. Environ. Microbiol. 64:46434649.
134. Rickard, A. H.,, R. J. Palmer,, Jr.,, D. S. Blehert,, S. R. Campagna,, M. F. Semmelhack,, P. G. Egland,, B. L. Bassler, and, P. E. Kolenbrander. 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60:14461456.
135. Rollins, D. M., and, R. R. Colwell. 1986. Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Appl. Environ. Microbiol. 52:531538.
136. Rollins, D. M.,, J. C. Coolbaugh,, R. I. Walker, and, E. Weiss. 1983. Biphasic culture system for rapid Campylobacter cultivation. Appl. Environ. Microbiol. 45:284289.
137. Romling, U. 2005. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life. Sci. 62:12341246.
138. Romling, U., and, D. Amikam. 2006. Cyclic di-GMP as a second messenger. Curr. Opin. Microbiol. 9:218228.
139. Saha, S. K., and, S. C. Sanyal. 1991. Better preservation of Campylobacter jejuni/C. coli in a defined medium. Indian J. Med. Res. 93:2628.
140. Sampathkumar, B.,, S. Napper,, C. D. Carrillo,, P. Willson,, E. Taboada,, J. H. Nash,, A. A. Potter,, L. A. Babiuk, and, B. J. Allan. 2006. Transcriptional and translational expression patterns associated with immobilized growth of Campylobacter jejuni. Microbiology 152:567577.
141. Sanders, S. Q.,, D. H. Boothe,, J. F. Frank, and, J. W. Arnold. 2007. Culture and detection of Campylobacter jejuni within mixed microbial populations of biofilms on stainless steel. J. Food Prot. 70:13791385.
142. Smibert, R. M. 1978. The genus Campylobacter. Annu. Rev. Microbiol. 32:673709.
143. Snelling, W. J.,, J. P. McKenna,, D. M. Lecky, and, J. S. Dooley. 2005. Survival of Campylobacter jejuni in waterborne protozoa. Appl. Environ. Microbiol. 71:55605571.
144. Somers, E. B.,, J. L. Schoeni, and, A. C. Wong. 1994. Effect of trisodium phosphate on biofilm and planktonic cells of Campylobacter jejuni, Escherichia coli O157: H7, Listeria monocytogenes and Salmonella typhimurium. Int. J. Food Microbiol. 22:2692676.
145. Stark, R. M.,, G. J. Gerwig,, R. S. Pitman,, L. F. Potts,, N. A. Williams,, J. Greenman,, I. P. Weinzweig,, T. R. Hirst, and, M. R. Millar. 1999. Biofilm formation by Helicobacter pylori. Lett. Appl. Microbiol. 28:121126.
146. Stead, D., and, S. F. Park. 2000. Roles of Fe superoxide dismutase and catalase in resistance of Campylobacter coli to freeze-thaw stress. Appl. Environ. Microbiol. 66:31103112.
147. Stern, N. J. 1994. Mucosal competitive exclusion to diminish colonization of chickens by Campylobacter jejuni. Poult. Sci. 73:402407.
148. Stintzi, A. 2003. Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J. Bacteriol. 185:20092016.
149. Su, C. C.,, F. Shi,, R. Gu,, M. Li,, G. McDermott,, E. W. Yu, and, Q. Zhang. 2007. Preliminary structural studies of the transcriptional regulator CmeR from Campylobacter jejuni. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 63:3436.
150. Talibart, R.,, M. Denis,, A. Castillo,, J. M. Cappelier, and, G. Ermel. 2000. Survival and recovery of viable but noncultivable forms of Campylobacter in aqueous microcosm. Int. J. Food Microbiol. 55:263267.
151. Tangwatcharin, P.,, S. Chanthachum,, P. Khopaibool,, J. R. Chambers, and, M. W. Griffiths. 2007. Media for the aerobic resuscitation of Campylobacter jejuni. J. Food Prot. 70:10991109.
152. Tangwatcharin, P.,, S. Chanthachum,, P. Khopaibool, and, M. W. Griffiths. 2006. Morphological and physiological responses of Campylobacter jejuni to stress. J. Food Prot. 69:27472753.
153. Terzieva, S. I., and, G. A. McFeters. 1991. Survival and injury of Escherichia coli, Campylobacter jejuni, and Yersinia enterocolitica in stream water. Can. J. Microbiol. 37:785790.
154. Thies, F. L.,, H. P. Hartung, and, G. Giegerich. 1998. Cloning and expression of the Campylobacter jejuni lon gene detected by RNA arbitrarily primed PCR. FEMS Microbiol. Lett. 165:329334.
155. Thies, F. L.,, H. Karch,, H. P. Hartung, and, G. Giegerich. 1999a. Cloning and expression of the dnaK gene of Campylobacter jejuni and antigenicity of heat shock protein 70. Infect. Immun. 67:11941200.
156. Thies, F. L.,, H. Karch,, H. P. Hartung, and, G. Giegerich. 1999b. The ClpB protein from Campylobacter jejuni: molecular characterization of the encoding gene and antigenicity of the recombinant protein. Gene 230:6167.
157. Thies, F. L.,, A. Weishaupt,, H. Karch,, H. P. Hartung, and, G. Giegerich. 1999c. Cloning, sequencing and molecular analysis of the Campylobacter jejuni groESL bicistronic operon. Microbiology 145(Pt. 1):8998.
158. Tholozan, J. L.,, J. M. Cappelier,, J. P. Tissier,, G. Delattre, and, M. Federighi. 1999. Physiological characterization of viable-but-nonculturable Campylobacter jejuni cells. Appl. Environ. Microbiol. 65:11101116.
159. Thomas, C.,, D. J. Hill, and, M. Mabey. 1999. Morphological changes of synchronized Campylobacter jejuni populations during growth in single phase liquid culture. Lett. Appl. Microbiol. 28:194198.
160. Trachoo, N., and, J. F. Frank. 2002. Effectiveness of chemical sanitizers against Campylobacter jejuni–containing biofilms. J. Food Prot. 65:11171121.
161. Trachoo, N.,, J. F. Frank, and, N. J. Stern. 2002. Survival of Campylobacter jejuni in biofilms isolated from chicken houses. J. Food Prot. 65:11101116.
162. Ulett, G. C.,, J. Valle,, C. Beloin,, O. Sherlock,, J. M. Ghigo, and, M. A. Schembri. 2007. Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect. Immun. 75:32333244.
163. van de Giessen, A. W.,, C. J. Heuvelman,, T. Abee, and, W. C. Hazeleger. 1996. Experimental studies on the infectivity of nonculturable forms of Campylobacter spp. in chicks and mice. Epidemiol. Infect. 117:4634670.
164. van Vliet, A. H.,, M. L. Baillon,, C. W. Penn, and, J. M. Ketley. 1999. Campylobacter jejuni contains two fur homologs: characterization of iron-responsive regulation of peroxide stress defense genes by the PerR repressor. J. Bacteriol. 181:63716376.
165. van Vliet, A. H.,, M. A. Baillon,, C. W. Penn, and, J. M. Ketley. 2001. The iron-induced ferredoxin FdxA of Campylobacter jejuni is involved in aerotolerance. FEMS Microbiol. Lett. 196:189193.
166. Vandamme, P. 2000. Taxonomy of the family Campylobacteraceae, p. 326. In I. Nachamkin and, M. J. Blaser (ed.), Campylobacter, 2nd ed. ASM Press, Washington, DC.
167. Withey, J. H., and, D. I. Friedman. 2003. A salvage pathway for protein structures: tmRNA and trans-translation. Annu. Rev. Microbiol. 57:101123.
168. Wolfe, A. J.,, D. E. Chang,, J. D. Walker,, J. E. Seitz-Partridge,, M. D. Vidaurri,, C. F. Lange,, B. M. Pruss,, M. C. Henk,, J. C. Larkin, and, T. Conway. 2003. Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol. Microbiol. 48:977988.
169. Zimmer, M.,, H. Barnhart,, U. Idris, and, M. D. Lee. 2003. Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens. Avian Dis. 47:101107.
170. Ziprin, R. L.,, R. E. Droleskey,, M. E. Hume, and, R. B. Harvey. 2003. Failure of viable nonculturable Campylobacter jejuni to colonize the cecum of newly hatched leghorn chicks. Avian Dis. 47:753758.
171. Ziprin, R. L., and, R. B. Harvey. 2004. Inability of cecal microflora to promote reversion of viable nonculturable Campylobacter jejuni. Avian Dis. 48:647650.

Tables

Generic image for table
Table 1.

Characterized and putative stress response genes in

Citation: Svensson S, Frirdich E, Gaynor E. 2008. Survival Strategies of : Stress Responses, the Viable but Nonculturable State, and Biofilms, p 571-590. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch32

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error