Specific and rapid enumeration of viable but nonculturable and viable-culturable gram-negative bacteria by using flow cytometry

Applied and Environmental Microbiology

Volumn 76, Issue 15, 2010, Pages 5088-5096

  Taimur Khan, Mohiuddin M ^a   Pyle, Barry H ^b   Camper, Anne K ^c  

^a University of New Mexico   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c Montana State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL TECHNIQUES; BACTERIAL CELLS; CULTURE METHODS; DAMAGED CELLS; DIRECT VIABLE COUNTS; EPIFLUORESCENCE MICROSCOPY; ESCHERICHIA COLI 0157:H7; FLOW-CYTOMETER; FLUORESCENT PROBES; GRAM-NEGATIVE BACTERIA; MOLECULAR METHODS; PHYSIOLOGICAL STATE; PROPIDIUM IODIDE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS SYRINGAE; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SAMPLE STORAGE; STAINING METHOD; VIABLE BUT NON-CULTURABLE;

BACTERIA; BACTERIOLOGY; CELL MEMBRANES; ESCHERICHIA COLI; FLOW CYTOMETRY;

CELL CULTURE;

FLUORESCENT DYE;

BACTERIUM; EXPERIMENTAL STUDY; FLOW CYTOMETRY; MICROSCOPY; PHYSIOLOGICAL RESPONSE;

ARTICLE; BACTERIAL COUNT; COMPARATIVE STUDY; ESCHERICHIA COLI O157; EVALUATION; FLOW CYTOMETRY; ISOLATION AND PURIFICATION; METABOLISM; METHODOLOGY; PSEUDOMONAS; SALMONELLA TYPHIMURIUM; STAINING; TIME; EVALUATION STUDY; PROCEDURES; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

COLONY COUNT, MICROBIAL; ESCHERICHIA COLI O157; FLOW CYTOMETRY; FLUORESCENT DYES; PSEUDOMONAS; SALMONELLA TYPHIMURIUM; STAINING AND LABELING; TIME FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI O157:H-; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS SYRINGAE; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 77955572486     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02932-09     Document Type: Article

References (58)

1. Atlas, R. M. 1997. Handbook of microbiological media. CRC Press, Boca Raton, FL.
2. Barer, M. R., L. T. Gribbon, C. R. Harwood, and C. E. Nwoguh. 1993. The viable but non-culturable hypothesis and medical bacteriology. Rev. Med. Microbiol. 4:183-191.
3. Barer, M. R., and C. R. Harwood. 1999. Bacterial viability and culturability, p. 93-137. In R. K. Poole (ed.), Advances in microbial physiology, vol. 41. Academic Press, London, United Kingdom.
4. Bercovier, H., M. Resnick, D. Kornitzer, and L. Levy. 1987. Rapid method for testing drug-susceptibility of Mycobacteria ssp. and gram-positive bacteria using rhodamine 123 and fluorescein diacetate. J. Microbiol. Methods 7:139-142.
5. Boulos, L., M. Prevost, B. Barbeau, J. Coallier, and R. Desjardins. 1999. LIVE/DEAD(R) BacLight(TM): application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J. Microbiol. Methods 37:77-86.
6. Brussaard, C. P. D. 2004. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microbiol. 70:1506-1513.
7. Chang, B., K. Sugiyama, T. Taguri, J. Amemura-Maekawa, F. Kura, and H. Watanabe. 2009. Specific detection of viable Legionella cells by combined use of photoactivated ethidium monoazide and FCR/real-time FCR. Appl. Environ. Microbiol. 75:147-153.
8. Davey, H. M., and D. B. Kell. 1996. Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiol. Rev. 60:641-696.
9. Delgado-Viscogliosi, P., T. Simonart, V. Parent, G. Marchand, M. Dobbelaere, E. Pierlot, V. Pierzo, F. M. Szczebara, E. G. Ferveur, K. Delabre, and J. M. Delattre. 2005. Rapid method for enumeration of viable Legionella pneumophila and other Legionella spp. in water. Appl. Environ. Microbiol. 71:4086-1096.
10. Gunasekera, T. S., P. V. Attfield, and D. A. Veal. 2000. A flow cytometry method for rapid detection and enumeration of total bacteria in milk. Appl. Environ. Microbiol. 66:1228-1232.
11. Hanna, S. E., C. J. Connor, and H. H. Wang. 2005. Real-time polymerase chain reaction for the food microbiologist: technologies, applications, and limitations. J. Food Sei. 70:R49-R53.
12. Herzenberg, L. A., D. Parks, B. Sahaf, O. Perez, and M. Roederer. 2002. The history and future of the fluorescence activated cell sorter and flow cytometry: a view from Stanford. Clin. Chem. 48:1819-1827.
13. Holloway, B. W. 1969. Genetics of Pseudomonas. Bacteriol. Rev. 33:419-443.
14. Horan, P. K., and J. W. Kappler. 1977. Automated fluorescent analysis for cytotoxicity assays. J. Immunol. Methods 18:309-316.
15. Hutter, K. J., and M. Stoehr. 1985. Detection and separation of the submetacentric marker chromosome of the WALKER (W-256) carcinoma using flow cytometiy and sorting. Histochemistry 82:469-475.
16. Joux, F., and P. LeBaron. 1997. Ecological implications of an improved direct viable count method for aquatic bacteria. Appl. Environ. Microbiol. 63:3643-3647.
17. Joux, F., and P. Lebaron. 2000. Use of fluorescent probes to assess physiological functions of bacteria at single-cell level. Microbes Infect. 2:15231535.
18. Karwoski, M. 1996. Automated direct and indirect methods in food microbiology: a literature review. Food Rev. Int. 12:155-174.
19. Kell, D. B., A. S. Kaprelyants, D. H. Weichart, C. R. Harwood, and M. R. Barer. 1998. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Van Leeuwenhoek 73:169-187.
20. Kogure, K., U. Simidu, and N. Taga. 1979. Tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25:415-420.
21. Kong, I.-S., T. C. Bates, A. Hulsmann, H. Hassan, B. E. Smith, and J. D. Oliver. 2004. Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol. Ecol. 50:133-142.
22. Leuko, S., A. Legat, S. Fendrihan, and H. Stan-Lotter. 2004. Evaluation of the LIVE/DEAD BacLight kit for detection of extremophilic archaea and visualization of microorganisms in environmental hypersaline samples. Appl. Environ. Microbiol. 70:6884-6886.
23. McDougald, D., S. A. Rice, D. Weichart, and S. Kjelleberg. 1998. Nonculturability: adaption or debilitation? FEMS Microbiol. Ecol. 25:1-9.
24. McFeters, G. A. 1990. Enumeration, occurrence, and significance of injured indicator bacteria in drinking water, p. 478-492. In G. A. McFeters (ed.), Drinking water microbiology: progress and recent developments. SpringerVerlag, New York, NY.
25. McFeters, G. A., M. W. Lechevallier, A. Singh, and J. S. Kippin. 1986. Health significance and occurrence of injured bacteria in drinking-water. Water Sci. Technol. 18:227-231.
26. Mossell, D. A. A., J. E. L. Corry, C. B. Struily, and R. M. Baird (ed.). 1995. Essentials of the microbiology of foods: a textbook for advanced studies, p. 96-106. John Wiley & Sons, Chichester, England.
27. Murphy, R. Y., B. L. Beard, E. M. Martin, L. K. Duncan, and J. A. Marcy. 2004. Comparative study of thermal inactivation of Escherichia coli 0157: H7, Salmonella, and Listeria monocytogenes in ground pork. J. Food Sci. 69:FMS97-FMS101.
28. Nader, W. F., C. T. Nebe, G. Nebe, A. Dastani, and C. Birr (ed.). 1991. Analysis of bacteria in environmental and medical microbiology by flow cytometry, p. 131-140. In A. Veheri, R. C. Tilton, and A. Barlow (ed.), Rapid methods and automation in microbiology and immunology. Springer-Verlag, Berlin, Germany.
29. Nebe-von Caron, G., and R. A. Badley. 1996. Bacterial characterization by flow cytometry, p. 257-290. In M. Al-Rubeai and A. N. Emeiy (ed.), Flow cytometry applications in cell culture. Marcel Dekker, New York, NY.
30. Nebe-von Caron, G., P. Stephens, and R. A. Badley. 1998. Assessment of bacterial viability status by flow cytometry and single cell sorting. J. Appl. Microbiol. 84:988-998.
31. Nebe-von-Caron, G., P. J. Stephens, C. J. Hewitt, J. R. Powell, and R. A. Badley. 2000. Analysis of bacterial function by multi-colour fluorescence flow cytometry and single cell sorting. J. Microbiol. Methods 42:97-114.
32. Nyström, T. 2001. Not quite dead enough: on bacterial life, culturability, senescence, and death. Arch. Microbiol. 176:159-164.
33. Oliver, J. D. (ed.) 1993. Formation of viable but nonculturable cells, p. 239-272. In S. Kjelleberg (ed.), Starvation in bacteria. Plenum Press, New York, NY.
34. Oliver, J. D. 2000. The public health significance of viable but nonculturable bacteria, p. 277-300. In R. R. Colwell and D. J. Grimes (ed.), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
35. Parthuisot, N., P. Catala, K. Lemarchand, J. Baudart, and P. Lebaron. 2000. Evaluation of ChemChrome V6 for bacterial viability assessment in waters. J. Appl. Microbiol. 89:370-380.
36. Pommepuy, M., M. Butin, A. Derrien, M. Gourmelon, R. R. Colwell, and M. Cormier. 1996. Retention of enteropathogenicity by viable but nonculturable Escherichia coli exposed to seawater and sunlight. Appl. Environ. Microbiol. 62:4621-4626.
37. Pore, R. S. 1994. Antibiotic susceptibility testing by flow-cytometiy. J. Antimicrob. Chemother. 34:613-627.
38. Pyle, B. H., S. C. Broadaway, and G. A. McFeters. 1995. A rapid, direct method for enumerating respiring enterohemorrhagic Escherichia coli 0157:H7 in water. Appl. Environ. Microbiol. 61:2614-2619.
39. Pyle, B. H., S. C. Broadaway, and G. A. McFeters. 1999. Sensitive detection of Escherichia coli 0157:H7 in food and water by immunomagnetic separation and solid-phase laser cytometiy. Appl. Environ. Microbiol. 65:19661972.
40. Rahman, I., M. Shahamat, M. A. R. Chowdhury, and R. R. Colwell. 1996. Potential virulence of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 62:115-120.
41. Reynolds, D. T., and C. R. Fricker. 1999. Application of laser scanning for the rapid and automated detection of bacteria in water samples. J. Appl. Microbiol. 86:785-795.
42. Rollié, S., and K. Sundmacher. 2008. Determination of cluster composition in heteroaggregation of binary particle systems by flow cytometiy. Langmuir 24:13348-13358.
43. Roszak, D. B., and R. R. Colwell. 1987. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51:365-379.
44. Roth, W. G., M. P. Leckie, and D. N. Dietzler. 1988. Restoration of colonyforming activity in osmotically stressed Escherichia coli by betaine. Appl. Environ. Microbiol. 54:3142-3146.
45. Sauch, J. F., D. Flanigan, M. L. Galvin, D. Berman, and W. Jakubowski. 1991. Propidium iodide as an indicator of Giardia cyst viability. Appl. Environ. Microbiol. 57:3243-3247.
46. Servais, P., H. Agogué, C. Courties, F. Joux, and P. Lebaron. 2001. Are the actively respiring cells (CTC+ ) those responsible for bacterial production in aquatic environments? FEMS Microbiol. Ecol. 35:171-179.
47. Shapiro, H. M. 1988. Practical flow cytometiy. Wiley-Liss, New York, NY.
48. Sherr, B. F., P. del Giorgio, and E. B. Sherr. 1999. Estimating abundance and single-cell characteristics of respiring bacteria via the redox dye CTC. Aquat. Microb. Ecol. 18:117-131.
49. Shin, J. H., F. S. Nolte, and C. J. Morrison. 1997. Rapid identification of Candida species in blood cultures by a clinically useful FCR method. J. Clin. Microbiol. 35:1454-1459.
50. Singh, A., and G. A. McFeters. 1986. Recovery, growth, and production of heat-stable enterotoxin by Escherichia coli after copper-induced injur;'. Appl. Environ. Microbiol. 51:738-742.
51. Smith, J. J., J. P. Howington, and G. A. McFeters. 1994. Survival, physiological response, and recoven' of enteric bacteria exposed to a polar marine environment. Appl. Environ. Microbiol. 60:2977-2984.
52. Stanley, E. C., R. J. Mole, R. J. Smith, S. M. Glenn, M. R. Barer, M. McGowan, and C. E. D. Rees. 2007. Development of a new, combined rapid method using phage and FCR for detection and identification of viable Mycobacterium paratuberculosis bacteria within 48 hours. Appl. Environ. Microbiol. 73:1851-1857.
53. Vasavada, P. C., and C. H. White. 1993. Symposium: developing methodology for microbial evaluation of milk and dairy products. J. Dairy Sci. 76: 3099-3100.
54. Verthé, K., and W. Verstraete. 2006. Use of flow cytometiy for analysis of phage-mediated killing of Enterobacter aerogenes. Res. Microbiol. 157:613618.
55. Völsch, A., W. F. Nader, H. K. Geiss, G. Nebe, and C. Birr. 1990. Detection and analysis of two serotypes of ammonia-oxidizing bacteria in sewage plants by flow cytometiy. Appl. Environ. Microbiol. 56:2430-2435.
56. Wallner, G., R. Amann, and W. Beisker. 1993. Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14:136-143.
57. Wu, X. Q., J. X. Zhang, J. Q. Liang, Y. Lu, H. M. Li, C. H. Li, J. Yue, L. S. Zhang, and Z. H. Liu. 2007. Comparison of three methods for rapid identification of mycobacterial clinical isolates to the species level. J. Clin. Microbiol. 45:1898-1903.
58. Yokomaku, D., N. Yamaguchi, and R. Nasu. 2000. Improved direct viable count procedure for quantitative estimation of bacterial viability in freshwater environments. Appl. Environ. Microbiol. 66:5544-5548.