State transitions of Vibrio parahaemolyticus VBNC cells evaluated by flow cytometry

Cytometry Part B - Clinical Cytometry

Volumn 74, Issue 5, 2008, Pages 272-281

  Falcioni, Tania ^a,b   Papa, Stefano ^a   Campana, Raffaella ^a   Manti, Anita ^a   Battistelli, Michela ^a   Baffone, Wally ^a  

^a UNIVERSITY OF URBINO   (Italy)

^b UNIVERSITY OF LLEIDA   (Spain)

Author keywords

Flow cytometry; Immunofluorescence; State transitions; Viability; Vibrio parahemolyticus VBNC

Indexed keywords

NUCLEIC ACID; PROPIDIUM IODIDE;

AGING; ANTIBODY AFFINITY; ARTICLE; BACTERIAL CELL; CELL COUNT; CELL CULTURE; CELL DAMAGE; CELL DEATH; CELL POPULATION; CELL RESPIRATION; CELL SIZE; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOFLUOROMETRY; EPIFLUORESCENCE MICROSCOPY; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; LIGHT SCATTERING; MICROCOSM; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; VIBRIO PARAHAEMOLYTICUS;

ANIMALS; ANTIBODIES; DNA, BACTERIAL; FLOW CYTOMETRY; HUMANS; MICE; MICE, INBRED BALB C; MICROBIAL VIABILITY; VIBRIO PARAHAEMOLYTICUS;

EID: 51749088303     PISSN: 15524949     EISSN: 15524957     Source Type: Journal    
DOI: 10.1002/cyto.b.20427     Document Type: Article

References (50)

1. Kiiyukia C, Venkateswaran K, Navarro M, Nakano H, Kawakami H, Hashimoto H. Seasonal distribution of Vibrio parahaemolyticus serotypes along the oyster beds in Hiroshima coast. J Fac Appl Biol Sci 1989;28:49-61.
2. Chakraborty S, Nair GB, Shinoda S. Pathogenic Vibrios in the natural aquatic environment. Rev Environ Health 1997;12:63-80.
3. DePaola A, Nordstrom JL, Bowers JC, Wells JG, Cook DW. Seasonal abundance of total and pathogenic Vibrio parahaemolyticus in Alabama oysters. Appl Environ Microbiol 2003;69:1521-1526.
4. Lozano-Leon A, Torres J, Osorio CR, Martinez-Urtaza J. Identification of TDH-positive Vibrio parahaemolyticus from an outbreak associated with raw oyster consumption in Spain. FEMS Microbiol Lett 2003;226:281-284.
5. Rippey SR. Infections diseases associated with molluscan shellfish consumption. Clin Microbiol Rev 1994;7:419-425.
6. Colwell RR. Global climate and infectious disease: The cholera paradigm. Science 1996;274:2025-2031.
7. Colwell RR.Bacterial death revisited. In:Colwell RR,Grimes DJ, editors. Nonculturable Microrganisms in the Environment. Washington, DC:American Society for Microbiology; 2000. pp 325-342.
8. Pommepuy M, Butin M, Derrien A, Gourmelon M, Colwell RR. Retention of enteropathogenicity by viable but nonculturable Escherichia coli exposed to sea water and sunlight. Appl Environ Microbiol 1996;62:4621-4626.
9. Baffone W, Citterio B, Vittoria E, Casaroli A, Campana R, Falzano L, Donelli G. Retention of virulence in viable but non-culturable halophilic Vibrio spp. Int J Food Microbiol 2003;89:31-39.
10. Jiang X, Chai TJ. Survival of Vibrio parahaemolyticus at low temperature under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl Environ Microbiol 1996;62:1300-1305.
11. Oliver JD. The public health significance of viable but non culturable bacteria. In:Colwell RR, Grimes DJ, editors. Nonculturable Microorganisms in the Environment.. Washington, DC: American Society for Microbiology; 2000. pp 277-300.
12. Wang G, Doyle MP. Survival of enterohemorrhagic Escherichia coli O157:H7 in water. J Food Prot 1998;61:662-667.
13. Tangwatcharin P, Chanthachum S, Khopaibool P, Griffiths MW. Morphological and physiological responses of Campylobacter jejuni to stress. J Food Prot 2006;69:2747-2753.
14. Wong HC, Shen CT, Chang CN, Lee YS, Oliver JD. Biochemical and virulence characterization of viable but nonculturable cells of Vibrio parahaemolyticus. J Food Prot 2004;67:2430-2435.
15. Delong EF, Wickham GS, Pace NR. Phylogenetic strains-ribosomal RNA based probes for the identification of single cells. Science 1989;243:1360-1363.
16. Oliver JD. The viable but nonculturable state in bacteria. J Microbiol 2005;43:93-100.
17. Smith B, Oliver JD. In situ and in vitro gene expression by Vibrio vulnificus during entry into, persistence within, and resuscitation from the viable but nonculturable state. Appl Environ Microbiol 2006;72:1445-1451.
18. Mason DJ, Lopez-Amoros R, Allman R, Stark JM, Lloyd D. The ability of membrane potential dyes and calcafluor with to distinguish between viable but nonviable bacteria. J Appl Bacteriol 1995;78: 309-315.
19. Joux F, Lebaron P. Use of fluorescent probes to assess physiological functions of bacteria at single-cell level. Microbes Infect 2000;2: 1523-1535.
20. Creach V, Baudoux AC, Bertru G, Le Rouzic B. Direct estimate of active bacteria: CTC use and limitations. J Microbiol Methods 2003;52:19-28.
21. Nebe-Von Caron G, Badley RA. Viability assessment of bacteria in mixed populations using flow cytometry. J Microsc 1995;179:55-66.
22. Nebe-Von Caron G, Stephens G, Hewitt PJ, Powell CJ, Badley RA. Analysis of bacterial function by multi-colour fluorescence flow cytometry and single cell sorting. J Microbiol Methods 2000;42:97-114.
23. Edwards C. Some problems posed by natural environments for monitoring microorganisms. In: Edwards C, editor. Envirorunetital Monitoting of Bacteria. New Jersey: Humana Press; 1999. pp 1-14.
24. Davey MH, Winson MK. Using flow cytometry to quantify microbial heterogeneity. Curr Issues Mol Biol 2003;5:9-15.
25. Steen HB, Boye E, Skarstad K, Bloom B, Godal T, Mustafa S. Applications of flow cytometry on bacteria: Cell cycle kinetics, drug effects and quantitation of antibody binding. Cytometry 1982;2:249-257.
26. Eitzman PD, Hendrick JL, Srienc F. Quantitative immunofluorescence in single Saccharomyces cerevisiae cells. Cytometry 1989;10: 475-483.
27. Chaffin WJ, Ringlet L, Larsen HS. Interactions of monospecific antisera with cell surface determinants of Candida albicans. Infect Imm 1988;56:3294-3296.
28. Mleczko J, Litke LL, Larsen HS, Chaffin WL. Effect of glutaraldehyde fixation on cell surface binding capacity of Candida albicans. Infect Imm 1989;57:3247-3249.
29. Porter J, Robinson J, Pickup R, Edwards C. Recovery of bacterial sub-population from seawage using immunofluorescent How cytometry and cell sorting. FEMS Microbiol Lett 1995;133:195-199.
30. Porter J, Pickup RW. Nucleic acid-based fluorescent probes in microbial ecology: Application of flow cytometry. J Microbiol Methods 2000;42:75-79.
31. Veal DA, Deere D, Ferrari B, Piper J, Attfield PV. Fluorescence staining and flow cytometry for monitoring microbial cells. J Immunol Methods 2000;243:191-210.
32. Mizunoe Y, Wai SN, Ishikawa T, Takade A, Yoshida SI. Resuscitation of viable but nonculturable cells of Vibrio parahaemolyticus induced at low temperature under starvation. FEMS Microbiol Lett 2000;186:115-120.
33. Wong HC, Wang P, Chen SY, Chiu SW. Resuscitation of viable but non-culturable Vibrio parahaemolyticus in a minimum salt medium. FEMS Microbiol Lett 2004;233:269-275.
34. Wolf PW, Oliver JD. Temperature effects on the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol Ecol 1992;101: 33-39.
35. Bates TC, Oliver JD. The viable but nonculturable state of Kanagawa positive and negative strains of Vibrio parahaemolyticus. J Microbiol 2004;42:74-79.
36. Whitesides MD, Oliver JD. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. Appl Environ Microbiol 1997;63: 1002-1005.
37. Baffone W, Casaroli A, Citterio B, Pierfelici L, Campana R, Vittoria E, Guaglianone E, Donelli G, Campylobacter jejuni loss of culturability in aqueous microcosms and ability to resuscitate in a mouse model. Int J Food Microbiol 2006;107:83-91.
38. Barbesti S, Citterio S, Labra M, Baroni MD, Neri MG, Sgorbati S. Two-and three-color fluorescence flow cytometric analysis of immunoidentified viable bacteria. Cytometry 2000;40:214-218.
39. Gasol JM, Zweifel UL, Peters F, Fuhrman JA, Hagström A. Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl Environ Microbiol 1999;65:4475-4483.
40. Falcioni T, Papa S, Campana R, Mannello F, Casaroli A, Burattini S, Baffone W. Flow cytometric evaluation of Vibrio parahaemolyticus adhesion inhibition to human epithelial cells. Cytometry B Clin Cytom 2005;66:25-35.
41. Battistelli M, De Sanctis R, De Bellis R, Cucchiarini L, Dachà M, Gobbi P. Rhodiola rosea as antioxidant in red blood cells: Ultrastructural and haemolytic behaviour. Eur J Histochem 2005;49:243-254.
42. Yamamoto H. Viable but non culturable state as general phenomenon of non-spore-forming bacteria, and its modelling. J Infect Chemother 2000;6:112-114.
43. Wong HC, Wang P. Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J Appl Microbiol 2004;96:359-366.
44. Berney M, Hammes F, Bosshard F, Weilemnann, HU, Egli T. Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight kit in combination with flow cytometry. Appl Environ Microbiol 2007;73:3283-3290.
45. Hoefel D, Grooby WL, Monis PT, Andrews S, Saint CP. Enumeration of water-borne bacteria using viability assays and flow cytometry: A comparison to culture-based techniques. J Microbiol Methods 2003; 55:585-597.
46. Berney M, Weilenmann HU, Egli T. Flow-cytometric study of vital cellular functions in Escherichia coli during solar disinfection (SODIS). Microbiology 2006;152:1719-1729.
47. Joux F, Lebaron P, Troussellier M, Succession of cellular states in a Salmonella typhimurium population during starvation in artificial seawater microcosms. FEMS Microbiol Ecol 1997;22:65-76.
48. Lebaron P, Servais P, Agogué H, Courties C, Joux F. Does the High Nucleic Content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl Environ Microbiol 2001;67:1775-1782.
49. Zampino D, Zaccone R, La Ferla R. Determination of living and active bacterioplankton: A comparison of methods. Chem Ecol 2004;20:411-422.
50. Gonzáles-Escalona N, Fey A, Höfle MG, Espero RT, Guzmán CA. Quantitative reverse transcription polymerase chain reaction analyses of Vibrio cholerae cells entering the viable but non-culturable state and starvation in response to cold shock. Environ Microbiol 2006;8:658-666.