Physiological characterization of viable-but-nonculturable Campylobacter jejuni cells

Applied and Environmental Microbiology

Volumn 65, Issue 3, 1999, Pages 1110-1116

  Tholozan, J L ^a   Cappelier, J M ^b   Tissier, J P ^a   Delattre, G ^a   Federighi, M ^b  

^a CEMAGREF   (France)

^b LUNAM UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE;

ARTICLE; BACTERIUM CULTURE; BACTERIUM TRANSFORMATION; CAMPYLOBACTER JEJUNI; CELL ENERGY; CELL MEMBRANE POTENTIAL; CELL PH; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CELL VOLUME; NONHUMAN; POTASSIUM CELL LEVEL; SODIUM CELL LEVEL; STRAIN DIFFERENCE;

CAMPYLOBACTER JEJUNI;

EID: 0032986394     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/aem.65.3.1110-1116.1999     Document Type: Article

References (67)

1. Amy, P. S., C. Pauling, and R. Y. Morita. 1983. Starvation-survival processes of a marine Vibrio. Appl. Environ. Microbiol. 45:1041-1048.
2. + transport systems ir prokaryotes, p. 205-224. In E. P. Bakker (ed.), Alkali cation transport systems in prokaryotes. CRC Press, Boca Raton, Fla.
3. + uptake systems, p. 253-276. In E. P. Bakker (ed.), Alkali cation transport systems in prokaryotes. CRC Press, Boca Raton, Fla.
4. Bakker, E. P., H. Rottenberg, and S. R. Caplan. 1976. An estimation of the light-induced electrochemical potential difference of protons across the membrane of Halobacterium halobium. Biochim. Biophys. Acta 440:557-572.
5. Booth, I. R., W. J. Mitchell, and W. A. Hamilton. 1979. Quantitative analysis of proton-linked transport systems. The lactose permease of Escherichia coli. Biochem. J. 182:687-696.
6. Bovill, R. A., and B. M. Mackey. 1997. Resuscitation of "non-culturable" cells from aged cultures of Campylobacter jejuni. Microbiology 143:1575-1581.
7. Boylen, C. W., and J. C. Ensign. 1970. Long-term starvation-survival of rod and spherical cells of Arthrobacter crystallopoites. J. Bacteriol. 103:569-577.
8. Cappelier, J. M., B. Lazaro, A. Rossero, A. Fernandez-Astorga, and M. Federighi. 1997. Double staining CTC/DAPI to detect and count viable but nonculturable Campylobacter jejuni cells. Vet. Res. 28:547-555.
9. Cappelier, J. M., and M. Federighi. 1998. Demonstration of viable but nonculturable state for Campylobacter jejuni. Rev. Med. Vet. 149:319-326.
10. Colwell, R. R., P. R. Brayton, D. J. Grimes, D. B. Roszak, S. A. Hug, and L. M. Palmer. 1985. Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms. Bio/Technology 3:817-820.
11. Crescentini, G., and V. Stocchi. 1984. Fast reversed-phase high-performance liquid chromatographic determination of nucleotides in red blood cells. J. Chromatogr. 290:393-399.
12. Dinnbier, U., E. Limpinsel, R. Schid, and E. P. Bakker. 1988. Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations. Arch. Microbiol. 150:348-357.
13. Epstein, W. 1986. Osmoregulation by potassium transport in Escherichia coli. FEMS Microbiol. Rev. 39:73-78.
14. Epstein, W., and B. S. Kim. 1971. Potassium transport loci in Escherichia coli K-12. J. Bacteriol. 108:639-643.
15. Federighi, M., J. L. Tholozan, J. M. Cappelier, J. P. Tissier, and J. L. Jouve. 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 Microbiol. 15:539-550.
16. Franzen, J. S., and S. B. Binkley. 1961. Comparison of the acid-soluble nucleotides in Escherichia coli at different growth rates. J. Biol. Chem. 236: 515-519.
17. 31P-NMR spectroscopy. Can. J. Microbiol. 39: 180-186.
18. Graber, M. L., D. C. Dilillo, B. L. Friedman, and E. Pastoriza-Munoz. 1986. Characteristics of fluoroprobes for measuring intracellular pH. Anal. Biochem. 154:202-212.
19. Guerlava, P., S. Nolf, and J. L. Tholozan. 1998. Rapid cooling, moderate heat treatment and nisin addition influence cell homeostasis of Clostridium perfringens type A. Int. J. Food Microbiol. 195-203.
20. Hamilton, R. D., and O. Holm-Hansen. 1967. Adenosine triphosphate content of marine bacteria. Limnol. Oceanogr. 12:319-324.
21. Harrison, D. E. F., and P. K. Maitra. 1969. Control of respiration and metabolism in growing Klebsiella aerogenes. The role of adenine nucleotides. Biochem. J. 112:647-656.
22. Hazeleger, W., C. Arkesleil, A. Toorop-Bouma, and R. Beumer. 1994. Detection of coccoid form of Campylobacter jejuni in chicken products with the use of the polymerase chain reaction. Food Microbiol. 24:273-281.
23. Horan, N. J., M. Midgley, and E. A. Dawes. 1981. Effects of starvation on transport, membrane potential and survival of Staphylococcus epidermidis under anaerobic conditions. J. Gen. Microbiol. 127:223-230.
24. Hussong, D., R. R. Colwell, M. O'Brien, E. Weiss, A. D. Pearson, R. M. Weiner, and W. D. Burge. 1987. Viable Legionella pneumophilla not detected by culture on agar media. Bio/Technology 5:947-950.
25. Jakubczak, E., and H. Leclerc. 1980. Mesure de l'ATP bactérien par bioluminescence: étude critique des méthodes d'extraction. Ann. Biol. Clin. 38: 297-304.
26. Jones, D. M., E. M. Sutcliffe, and A. Curry. 1991. Recovery of viable but non-culturable Campylobacter jejuni. J. Gen. Microbiol. 137:2477-2482.
27. Karl, D. M. 1980. Cellular nucleotide measurements and application to the microbial loop. Microbiol. Rev. 44:739-796.
28. Knowles, C. J. 1977. Microbial metabolic regulation by adenine nucleotide pools. Symp. Soc. Gen. Microbiol. 27:241-283.
29. Kobs, M. 1995. A procedure for preparing microscopic organisms for SEM. Eur. Microsc. Anal. 35:25.
30. Kogure, K., V. Sindu, and N. Taga. 1979. A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25:415-420.
31. Liao, C. L., and D. E. Atkinson. 1971. Regulation at the phosphoenolpyruvate branchpoint in Azotobacter vinelandii: pyruvate kinase. J. Bacteriol. 106: 37-44.
32. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 163:265-275.
33. MacDonnell, M. T., and M. A. Hood. 1982. Isolation and characterization of ultramicrobacteria from a Gulf Coast estuary. Appl. Environ. Microbiol. 43: 566-571.
34. 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. 72:512-516.
35. Miguelez, E., and D. J. Gilmour. 1994. Regulation of cell volume in the salt tolerant bacterium Halomonas elongata. Lett. Appl. Bacteriol. 19:363-365.
36. Moriarty, D. J. W., and K. T. Bell. 1993. Bacterial growth and starvation in aquatic environments, p. 25-53. In S. Kjelleberg (ed.), Starvation in bacteria. Plenum Press, New York, N.Y.
37. Morita, R. Y. 1997. Estimating nutrient bioavailability for microbes, p. 135-192. In C. A. Reddy, A. M. Chakrabarty, A. L. Demain, and J. M. Tiedje (ed.), Bacteria in oligotrophic environments. Chapman and Hall, New York, N.Y.
38. Morita, R. Y. 1997. Physiology of starvation-survival, p. 274-350. In C. A. Reddy, A. M. Chakrabarty, A. L. Demain, and J. M. Tiedje (ed.), Bacteria in oligotrophic environments. Chapman and Hall, New York, N.Y.
39. Noel, J., A. Tejedor, P. Vinay, and R. Laprade. 1989. Fluorescence measurements of intracellular pH on proximal tubule suspensions: the need for a BCECF sink. Renal Physiol. Biochem. 12:371-387.
40. Notermans, S., and H. Hoogenboom-Verdegaal. 1992. Existing and emerging foodborne diseases. Int. J. Food Microbiol. 15:197-205.
41. Novitsky, J. A., and R. Y. Morita. 1976. Morphological characterization of small cells resulting from nutrient starvation in a psychrophilic marine Vibrio. Appl. Environ. Microbiol. 32:619-622.
42. Oliver, J. D. 1993. Formation of viable but nonculturable cells, p. 239-272. In S. Kjelleberg (ed.), Starvation in bacteria. Plenum Press, New York, N.Y.
43. Otto, R., J. Vije, B. ten Brink, B. Klont, and W. N. Konings. 1985. Energy metabolism in Streptococcus cremoris during lactose starvation. Arch. Microbiol. 141:348-352.
44. Rahman, I., M. Shahamat, P. A. Kirchman, E. Russek-Cohen, and R. K. Colwell. 1994. Methionine uptake and cytopathogenicity of viable but non-culturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 60:3573-3578.
45. Ravel, J., I. T. Knight, C. E. Monohan, R. T. Hill, and R. R. Colwell. 1995. Temperature-induced recovery of Vibrio cholerae from the viable but non-culturable state: growth or resuscitation? Microbiology 141:377-383.
46. Richey, B., D. S. Cayley, M. C. Mossing, C. Kolka, C. V. Anderson, T. C. Farrar, and M. T. Record, Jr. 1987. Variability of the intracellular ionic environment of Escherichia coli. Differences between in vitro and in vivo effects of ion concentration on protein-DNA interactions and gene expression. J. Biol. Chem. 262:7157-7164.
47. Rodriguez, G. G., D. Philipps, K. Ishigmo, and H. F. Ridgway. 1992. Use of a fluorescent redox probe for direct visualization of actively respiring bacteria. Appl. Environ. Microbiol. 58:1801-1808.
48. Rollins, D. M., and R. R. Colwell. 1986. Viable but nonculturable stage of Campylobacter jejuni and its role in survival in natural, aquatic environment. Appl. Environ. Microbiol. 58:531-538.
49. Roszak, D. B., D. J. Grimes, and R. R. Colwell. 1984. Viable but non-recoverable stage of Salmonella enteritidis in aquatic systems. Can. J. Microbiol. 30:334-338.
50. Rottenberg, H. 1979. The measurement of membrane potential and ΔpH in cells, organelles, and vesicles. Methods Enzymol. 55:547-569.
51. Saha, S. K., S. Saha, and S. C. Sanyal. 1991. Recovery of injured Campylobacter jejuni cells after animal passage. Appl. Environ. Microbiol. 57:3388-3389.
52. Schön, G. 1969. Der Einfluss der Kulturbedingungen auf den ATP-, ADP-, and AMP-Spiegel bei Rhodospirillum rubrum. Arch. Mikrobiol. 66:348-364.
53. Schönheit, P., and H. J. Perski. 1983. ATP synthesis driven by a potassium diffusion potential in Methanobacterium thermoautotrophicum is stimulated by sodium. FEMS Microbiol. Lett. 15:69-74.
54. Severin, E., J. Stellmach, and H. M. Nachtigal. 1985. Fluorimetric assay of redox activity in cells. Anal. Chim. Acta 170:341-346.
55. Skirrow, M. B. 1990. Foodborne illness: Campylobacter. Lancet 336:921-923.
56. Smigielski, A. J., B. J. Wallace, and K. C. Marshall. 1989. Changes in membrane functions during short-term starvation of Vibro fluvialis strain NCTC 11328. Arch. Microbiol. 151:336-347.
57. Stern, N. J., D. M. Jones, I. V. Wesley, and D. M. Rollins. 1994. Colonization of chicks by nonculturable Campylobacter jejuni spp. Lett. Appl. Microbiol. 18:333-336.
58. Taylor, D. N. 1992. Campylobacter infections in developing countries, p. 20-30. In 1. Nachamkin, M. J. Blaser, and L. S. Tompkins (ed.), Campylobacter jejuni. Current topics and future trends. American Society for Microbiology, Washington, D.C.
59. Tsapis, A., and A. Kepes. 1977. Transient breakdown of the permeability barrier of the membrane of Escherichia coli upon hypoosmotic shock. Biochim. Biophys Acta 469:1-12.
60. Tsujimoto, K., M. Semadeni, M. Huflejt, and L. Packer. 1988. Intracellular pH of halobacteria can be determined by the fluorescent dye 2′,7′-bis(carboxyethyl)-5(6)-carboxyfluorescein. Biochem. Biophys. Res. Commun. 155: 123-129.
61. van Elsas, J. D., and L. S. van Overbeek. 1993. Bacterial response to soil stimuli, p. 55-79. In S. Kjelleberg (ed.), Starvation in bacteria. Plenum Press, New York, N.Y.
62. Walker-Simmons, M., and D. E. Atkinson. 1977. Functional capacities and the adenylate energy charge in Escherichia coli under conditions at nutritional stress. J. Bacteriol. 130:375-683.
63. Webster, J. J., G. J. Hampton, J. T. Wilson, W. C. Ghiorse, and F. R. Leach. 1985. Determination of microbial cell numbers in subsurface samples. Groundwater 23:17-25.
64. Xu, H. S., N. Roberts, F. L. Singleton, R. W. Attwell, D. J. Grimes, and R. R. Colwell. 1982. Survival and viability of non-culturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8: 313-323.
65. + regulated by extracellular pH in Escherichia coli. FEBS Lett. 120:125-127.
66. Zimmerman, R., R. Iturriaga, and J. Becker-Birck. 1978. Simultaneous determination of the total number of aquatic bacteria and the number thereof involved in respiration. Appl. Environ. Microbiol. 36:925-939.
67. Zychinsky, E., and A. Matin. 1983. Effect of starvation on cytoplasmic pH, proton motive force, and viability of an acidophilic bacterium, Thiobacillus acidophilus. J. Bacteriol. 153:371-374.