The importance of the viable but non-culturable state in human bacterial pathogens

Frontiers in Microbiology

Volumn 5, Issue JUN, 2014, Pages 1-1

  Li, Laam ^a   Mendis, Nilmini ^a   Trigui, Hana ^a   Oliver, James D ^b   Faucher, Sebastien P ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

Antibiotic; Biofilm; Human pathogens; Resuscitation; Stress; VBNC; Virulence

Indexed keywords

EID: 84905160775     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00258     Document Type: Review

References (224)

1. Abe, A., Ohashi, E., Ren, H., Hayashi, T., and Endo, H. (2007). Isolation and characterization of a cold-induced nonculturable suppression mutant of Vibrio vulnificus. Microbiol. Res. 162, 130-138. doi: 10.1016/j.micres.2006.01.007
2. Adams, B. L., Bates, T. C., and Oliver, J. D. (2003). Survival of Helicobacter pylori in a natural freshwater environment. Appl. Environ. Microbiol. 69, 7462-7466. doi: 10.1128/AEM.69.12.7462-7466.2003
3. Aiba, H., Nakasai, F., Mizushima, S., and Mizuno, T. (1989). Evidence for the physiological importance of the phosphotransfer between the two regulatory components, EnvZ and OmpR, in osmoregulation in Escherichia coli. J. Biol. Chem. 264, 14090-14094.
4. Al-Bana, B. H., Haddad, M. T., and Garduño, R. A. (2013). Stationary phase and mature infectious forms of Legionella pneumophila produce distinct viable but non-culturable cells. Environ. Microbiol. 2, 382-395. doi: 10.1111/1462-2920.12219
5. Alexander, E., Pham, D., and Steck, T. R. (1999). The viable-but-nonculturable condition is induced by copper in Agrobacterium tumefaciens and Rhizobium leguminosarum. Appl. Environ. Microbiol. 65, 3754-3756.
6. Allegra, S., Berger, F., Berthelot, P., Grattard, F., Pozzetto, B., and Riffard, S. (2008). Use of flow cytometry to monitor Legionella viability. Appl. Environ. Microbiol. 74, 7813-7816. doi: 10.1128/AEM.01364-08
7. Alleron, L., Khemiri, A., Koubar, M., Lacombe, C., Coquet, L., Cosette, P., et al. (2013). VBNC Legionella pneumophila cells are still able to produce virulence proteins. Water Res. 47, 6606-6617. doi: 10.1016/j.watres.2013.08.032
8. Alleron, L., Merlet, N., Lacombe, C., and Frère, J. (2008). Long-term survival of Legionella pneumophila in the viable but nonculturable state after monochloramine treatment. Curr. Microbiol. 57, 497-502. doi: 10.1007/s00284-008-9275-9
9. Altman, F. P. (1970). On the oxygen-sensitivity of various tetrazolium salts. Histochemie 22, 256-261. doi: 10.1007/bf00306103
10. Amato, S. M., Fazen, C. H., Henry, T., Mok, W. W., Orman, M. A., Sandvik, E. L., et al. (2014). The role of metabolism in bacterial persistence. Front. Microbiol. 5:70. doi: 10.3389/fmicb.2014.00070
11. Amel, B. K.N., Amine, B., and Amina, B. (2008). Survival of Vibrio fluvialis in seawater under starvation conditions. Microbiol. Res. 163, 323-328. doi: 10.1016/j.micres.2006.06.006
12. Anderson, L. F., Tamne, S., Watson, J. P., Cohen, T., Mitnick, C., Brown, T., et al. (2013). Treatment outcome of multi-drug resistant Tuberculosis in the United Kingdom: retrospective-prospective cohort study from 2004 to 2007. Euro. Surveill. 18:20601. doi: 10.2807/1560-7917.ES2013.18.40.20601
13. Anderson, M., Bollinger, D., Hagler, A., Hartwell, H., Rivers, B., Ward, K., et al. (2001). Viable but nonculturable bacteria are present in mouse and human urine specimens. J. Clin. Microbiol. 42, 753-758. doi: 10.1128/JCM.42.2.753-758.2004
14. Anuchin, A. M., Mulyukin, A. L., Suzina, N. E., Duda, V. I., El-Registan, G. I., and Kaprelyants, A. S. (2009). Dormant forms of Mycobacterium smegmatis with distinct morphology. Microbiology 155, 1071-1079. doi: 10.1099/mic.0.023028-0
15. Arana, I., Muela, A., Iriberri, J., Egea, L., and Barcina, I. (1992). Role of hydrogen peroxide in loss of culturability mediated by visible light in Escherichia coli in a freshwater ecosystem. Appl. Environ. Microbiol 58, 3903-3907.
16. Asakura, H., Ishiwa, A., Arakawa, E., Makino, S-I, Okada, Y., Yamamoto, S., et al. (2007a). Gene expression profile of Vibrio cholerae in the cold stress-induced viable but non-culturable state. Environ. Microbiol. 9, 869-879. doi: 10.1111/j.1462-2920.2006.01206.x
17. 157:H7 corresponds to the viable but non-culturable state. Res. Microbiol. 159, 709-717. doi: 10.1016/j.resmic.2008.08.005
18. 7 in the oxidation-induced viable but non-culturable state. Microbiol. Immunol. 51, 875. doi: 10.1111/j.1348-0421.2007.tb03969.x
19. Atluri, S., Ragkousi, K., Cortezzo, D. E., and Setlow, P. (2006). Cooperativity between different nutrient receptors in germination of spores of Bacillus subtilis and reduction of this cooperativity by alterations in the GerB receptor. J. Bacteriol. 188, 28-36. doi: 10.1128/JB.188.1.28-36.2006
20. Ayrapetyan, M., Williams, T. C., and Oliver, J. D. (2014). Inspecific quorum sensing mediates the resuscitation of viable but nonculturable vibrios. Appl. Environ. Microbiol. 80, 2478-2483. doi: 10.1128/AEM.00080-14
21. Baffone, W., Casaroli, A., Citterio, B., Pierfelici, L., Campana, R., Vittoria, E., et al. (2006). Campylobacter jejuni loss of culturability in aqueous microcosms and ability to resuscitate in a mouse model. Int. J. Food Microbiol. 107, 83-91. doi: 10.1016/j.ijfoodmicro.2005.08.015
22. Baffone, W., Citterio, B., Vittoria, E., Casaroli, A., Campana, R., Falzano, L., et al. (2003). Retention of virulence in viable but non-culturable halophilic Vibrio spp. Int. J. Food. Microbiol. 89, 31-39. doi: 10.1016/S0168-1605(03)00102-8
23. Banin, E., Israely, T., Kushmaro, A., Loya, Y., Orr, E., and Rosenberg, E. (2000). Penetration of the coral-bleaching bacterium Vibrio shiloi into Oculina patagonica. Appl. Environ. Microbiol. 66, 3031-3036. doi: 10.1128/AEM.66.7.3031-3036.2000
24. Barcina, I., Lebaron, P., and Vives-Rego, J. (1997). Survival of allochthonous bacteria in aquatic systems: a biological approach. FEMS Microbiol. Ecol. 23, 1-9. doi: 10.1111/j.1574-6941.1997.tb00385.x
25. Bates, T. C., and Oliver, J. D. (2004). The viable but nonculturable state of kanagawa positive and negative strains of Vibrio parahaemolyticus. J. Microbiol. 42, 74-79.
26. Besnard, V., Federighi, M., and Cappelier, J. M. (2000). Evidence of viable but non-culturable state in Listeria monocytogenes by direct viable count and CTC-DAPI double staining. Food Microbiol. 17, 697-704. doi: 10.1006/fmic.2000.0366
27. Besnard, V., Federighi, M., Declerq, E., Jugiau, F., and Cappelier, J. M. (2002). Environmental and physico-chemical factors induce VBNC state in Listeria monocytogenes. Vet. Res. 33, 359-370. doi: 10.1051/vetres:2002022
28. Biosca, E. G., Amaro, C., Marco-Noales, E., and Oliver, J. D. (1996). Effect of low temperature on starvation-survival of the eel pathogen Vibrio vulnificus biotype 2. Appl. Environ. Microbiol. 62, 450-455.
29. Birbari, W., Wright, A., and Rodrick, G. (2000). Viable but non-culturable response for phase variants of Vibrio vulnificus in clams. J. Shellfish Res. 19, 660.
30. Bloomfield, S. F., Stewart, G. S., Dodd, C. E., Booth, I. R., and Power, E. G. (1998). The viable but non-culturable phenomenon explained? Microbiology 144, 1-3. doi: 10.1099/00221287-144-1-1
31. Boaretti, M., Lleò, M. M., Bonato, B., Signoretto, C., and Canepari, P. (2003). Involvement of rpoS in the survival of Escherichia coli in the viable but non-culturable state. Environ. Microbiol. 5, 986-996. doi: 10.1046/j.1462-2920.2003.00497.x
32. Bogosian, G., Aardema, N. D., Bourneuf, E. V., Morris, P. J., and O'Neil, J. P. (2000). Recovery of hydrogen peroxide-sensitive culturable cells of Vibrio vulnificus gives the appearance of resuscitation from a viable but nonculturable state. J. Bacteriol. 182, 5070-5075. doi: 10.1128/JB.182.18.5070-5075.2000
33. Bovill, R. A., and Mackey, B. M. (1997). Resuscitation of 'non-culturable' cells from aged cultures of Campylobacter jejuni. Microbiology 143, 1575-1581.
34. Buck, J. (1979). "The plate count in aquatic microbiology," in Native Aquatic Bacteria: Enumeration, Activity and Ecology, eds J. W. Costerton, and R. R. Colwell (Philadelphia, PA: American Society for Testing and Materials), 19-28. doi: 10.1520/STP36000S
35. Buse, H. Y., Donohue, M. J., and Ashbolt, N. J. (2013). Hartmannella vermiformis inhibition of Legionella pneumophila cultivability. Microbiol. Ecol. 66, 715-726. doi: 10.1007/s00248-013-0250-z
36. Byrd, J. J., Xu, H. S., and Colwell, R. R. (1991). Viable but nonculturable bacteria in drinking water. Appl. Environ. Microbiol. 57, 875-878.
37. Cappelier, J. M., Besnard, V., Roche, S., Garrec, N., Zundel, E., Velge, P., et al. (2005). Avirulence of viable but non-culturable Listeria monocytogenes cells demonstrated by in vitro and in vivo models. Vet. Res. 36, 589-599. doi: 10.1051/vetres:2005018
38. Cappelier, J. M., Minet, J., Magras, C., Colwell, R. R., and Federighi, M. (1999). 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, 5154-5157.
39. Caro, A., Got, P., Lesne, J., Binard, S., and Baleux, B. (1999). Viability and virulence of experimentally stressed nonculturable Salmonella typhimurium. Appl. Environ. Microbiol. 65, 3229-3232.
40. Cashel, M., Gentry, D. R., Hernandez, V. J., and Vinella, D. (1996) "The stringent response," in Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, eds F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, et al. (Washington, DC: ASM Press), 1458-1496.
41. Cerca, F., Andrade, F., França, â., Andrade, E. B., Ribeiro, A., Almeida, A. A., et al. (2011). Staphylococcus epidermidis biofilms with higher proportions of dormant bacteria induce a lower activation of murine macrophages. J. Med. Microbiol. 60, 1717-1724. doi: 10.1099/jmm.0.031922-0
42. Charoenlap, N., Eiamphungporn, W., Chauvatcharin, N., Utamapongchai, S., Vattanaviboon, P., and Mongkolsuk, S. (2005). OxyR mediated compensatory expression between ahpC and katA and the significance of ahpC in protection from hydrogen peroxide in Xanthomonas campestris. FEMS Microbiol. Lett. 249, 73-78. doi: 10.1016/j.femsle.2005.06.002
43. Chatterji, D., Fujita, N., and Ishihama, A. (1998). The mediator for stringent control, ppGpp, binds to the ß-subunit of Escherichia coli RNA polymerase. Genes Cells 3, 279-287. doi: 10.1046/j.1365-2443.1998.00190.x
44. Chaveerach, P., ter Huurne, A. A. H. M., Lipman, L. J. A., and van Knapen, F. (2003). Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl. Environ. Microbiol. 69, 711-714. doi: 10.1128/AEM.69.1.711-714.2003
45. Cho, J.C., and Kim, S.J. (1999). Viable, but non-culturable, state of a green fluorescence protein-tagged environmental isolate of Salmonella typhi in groundwater and pond water. FEMS Microbiol. Lett. 170, 257-264. doi: 10.1111/j.1574-6968.1999.tb13382.x
46. Christman, M. F., Morgan, R. W., Jacobson, F. S., and Ames, B. N. (1985). Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41, 753-762. doi: 10.1016/S0092-8674(85)80056-8
47. Cohen-Gonsaud, M., Barthe, P., Bagneris, C., Henderson, B., Ward, J., Roumestand, C., et al. (2005). The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes. Nat. Struct. Mol. Biol. 12, 270-273. doi: 10.1038/nsmb905
48. Colwell, R. R., Brayton, P. R., Grimes, D. J., Roszak, D. B., Huq, S. A., and Palmer, L. M. (1985). Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms. Nat. Biotech. 3, 817-820. doi: 10.1038/nbt0985-817
49. Colwell, R. R., Brayton, P. R., Herrington, D., Tall, B., Huq, A., and Levine, M. M. (1996). Viable but non-culturable Vibrio cholerae O1 revert to a cultivable state in the human intestine. World J. Microbiol. Biotechnol. 12, 28-31. doi: 10.1007/BF00327795
50. Colwell, R. R., and Grimes, D. J. (2000). Nonculturable microorganisms in the environment. Herndon, VA: ASM press. doi: 10.1007/978-1-4757-0271-2
51. Cook, K. L., and Bolster, C. H. (2007). Survival of Campylobacter jejuni and Escherichia coli in groundwater during prolonged starvation at low temperatures. J. Appl. Microbiol. 103, 573-583. doi: 10.1111/j.1365-2672.2006.03285.x
52. Cools, I., Uyttendaele, M., Caro, C., D'Haese, E., Nelis, H. J., and Debevere, J. (2003). Survival of Campylobacter jejuni strains of different origin in drinking water. J. Appl. Microbiol. 94, 886-892. doi: 10.1046/j.1365-2672.2003.01916.x
53. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322. doi: 10.1126/science.284.5418.1318
54. Coutard, F., Lozach, S., Pommepuy, M., and Hervio-Heath, D. (2007). Real-time reverse transcription-PCR for transcriptional expression analysis of virulence and housekeeping genes in viable but nonculturable Vibrio parahaemolyticus after recovery of culturability. Appl. Environ. Microbiol. 73, 5183-5189. doi: 10.1128/aem.02776-06
55. Cronquist, A. B., Mody, R. K., Atkinson, R., Besser, J., D'Angelo, M. T., Hurd, S., et al. (2012). Impacts of culture-independent diagnostic practices on public health surveillance for bacterial enteric pathogens. Clin. Infect. Dis. 54 (Suppl. 5), S432-S439. doi: 10.1093/cid/cis267
56. Crowle, A. J., Dahl, R., Ross, E., and May, M. H. (1991). Evidence that vesicles containing living, virulent Mycobacterium tuberculosis or Mycobacterium avium in cultured human macrophages are not acidic. Infect. Immun. 59, 1823-1831.
57. Cunningham, E., O'Byrne, C., and Oliver, J. D. (2009). Effect of weak acids on Listeria monocytogenes survival: evidence for a viable but nonculturable state in response to low pH. Food Control 20, 1141-1144. doi: 10.1016/j.foodcont.2009.03.005
58. Cuny, C., Dukan, L., Fraysse, L., Ballesteros, M., and Dukan, S. (2005). Investigation of the first events leading to loss of culturability during Escherichia coli starvation: future nonculturable bacteria form a subpopulation. J. Bacteriol. 187, 2244-2248. doi: 10.1128/JB.187.7.2244-2248.2005
59. Darcan, C., Özkanca, R., Idil, ö., and Flint, K. P. (2009). Viable but non-culturable state (VBNC) of Escherichia coli related to EnvZ under the effect of pH, starvation and osmotic stress in sea water. Pol. J. Microbiol. 58, 307-317.
60. Day, A. P., and Oliver, J. D. (2004). Changes in membrane fatty acid composition during entry of Vibrio vulnificus into the viable but non-culturable state. J. Microbiol. 42, 69-73.
61. de Angelis, M., and Gobbetti, M. (2004). Environmental stress responses in Lactobacillus: a review. Proteomics 4, 106-122. doi: 10.1002/pmic.200300497
62. del Campo, R., Russi, P., Mara, P., Mara, H., Peyrou, M., de León, I. P., et al. (2009). Xanthomonas axonopodis pv. citri enters the VBNC state after copper treatment and retains its virulence. FEMS Microbiol. Lett. 298, 143-148, doi: 10.1111/j.1574-6968.2009.01709.x
63. Desnues, B., Cuny, C., Grégori, G., Dukan, S., Aguilaniu, H., and Nyström, T. (2003). Differential oxidative damage and expression of stress defence regulons in culturable and non-culturable Escherichia coli cells. EMBO Rep. 4, 400-404. doi: 10.1038/sj.embor.embor799
64. Dhiaf, A., Bakhrouf, A., and Witzel, K. (2008). Resuscitation of eleven-year VBNC Citrobacter. J. Water Health 6, 565-568. doi: 10.2166/wh.2008.131
65. 7 in the phyllosphere of lettuce: a food safety risk factor. Appl. Environ. Microbiol. 77, 8295-8302. doi: 10.1128/AEM.05020-11
66. Downing, K. J., Mischenko, V. V., Shleeva, M. O., Young, D. I., Young, M., Kaprelyants, A. S., et al. (2005). Mutants of Mycobacterium tuberculosis lacking three of the five rpf-Like genes are defective for growth in vivo and for resuscitation in vitro. Infect. Immun. 73, 3038-3043. doi: 10.1128/IAI.73.5.3038-3043.2005
67. Du, M., Chen, J., Zhang, X., Li, A., Li, Y., and Wang, Y. (2007). Retention of virulence in a viable but nonculturable Edwardsiella tarda isolate. Appl. Environ. Microbiol. 73, 1349-1354. doi: 10.1128/AEM.02243-06
68. Ducret, A., Chabalier, M., and Dukan, S. (2014). Characterization and resuscitation of 'non-culturable' cells of Legionella pneumophila. BMC Microbiol. 14:3. doi: 10.1186/1471-2180-14-3
69. Duffy, L. L., and Dykes, G. A. (2009). The ability of Campylobacter jejuni cells to attach to stainless steel does not change as they become nonculturable. Foodborne Pathog. Dis. 6, 631-634. doi: 10.1089/fpd.2008.0250
70. Dwidjosiswojo, Z., Richard, J., Moritz, M. M., Dopp, E., Flemming, H.C., and Wingender, J. (2011). Influence of copper ions on the viability and cytotoxicity of Pseudomonas aeruginosa under conditions relevant to drinking water environments. Int. J. Hyg. Environ. Health 214, 485-492. doi: 10.1016/j.ijheh.2011.06.004
71. Ehrlich, G. D., Veeh, R., Wang, X., Costerton, J. W., Hayes, J. D., Hu, F. Z., et al. (2002). Mucosal biofilm formation on middle-ear mucosa in the Chinchilla model of otitis media. J. Amer. Med. Assoc. 287, 1710-1715. doi: 10.1001/jama.287.13.1710
72. Epstein, S. S. (2009). Microbial awakenings. Nature 457, 1083. doi: 10.1038/4571083a
73. Fattorini, L., Piccaro, G., Mustazzolu, A., and Giannoni, F. (2013). Targeting dormant bacilli to fight tuberculosis. Mediterr. J. Hematol. Infect. Dis. 5, e2013072. doi: 10.4084/MJHID.2013.072
74. Fera, M. T., Maugeri, T. L., Gugliandolo, C., La Camera, E., Lentini, V., Favaloro, A., et al. (2008). Induction and resuscitation of viable nonculturable Arcobacter butzleri cells. Appl. Environ. Microbiol. 74, 3266-3268. doi: 10.1128/AEM.00059-08
75. Flemming, H.C., Percival, S. I., and Walker, J. T. (2002). Contamination potential of biofilms in water distribution systems. Water Sci. Technol. Water Suppl. 2, 271-280.
76. Forst, S., Comeau, D., Norioka, S., and Inouye, M. (1987). Localization and membrane topology of EnvZ, a protein involved in osmoregulation of OmpF and OmpC in Escherichia coli. J. Biol. Chem. 262, 16433-16438.
77. Freestone, P. P. E., Haigh, R. D., Williams, P. H., and Lyte, M. (1999). Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers. FEMS Microbiol. Lett. 172, 53-60. doi: 10.1111/j.1574-6968.1999.tb13449.x
78. Freestone, P. P. E., Williams, P. H., Lyte, M., and Haigh, R. D. (2001). E. coli, Salmonella or Hafnia autoinducers. US Pat. US 6,316,244 B1.
79. García, M. T., Jones, S., Pelaz, C., Millar, R. D., and Kwaik, Y. A. (2007). Acanthamoeba polyphaga resuscitates viable non-culturable Legionella pneumophila after disinfection. Environ. Microbiol. 9, 1267-1277. doi: 10.1111/j.1462-2920.2007.01245.x
80. Gengenbacher, M., and Kaufmann, S. H. E. (2012). Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol. Rev. 36, 514-532. doi: 10.1111/j.1574-6976.2012.00331.x
81. Gentry, D. R., Hernandez, V. J., Nguyen, L. H., Jensen, D. B., and Cashel, M. (1993). Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J. Bacteriol. 175, 7982-7989.
82. Ghezzi, J. I., and Steck, T. R. (1999). Induction of the viable but non-culturable condition in Xanthomonas campestris pv. campestris in liquid microcosms and sterile soil. FEMS Microbiol. Ecol. 30, 203-208. doi: 10.1111/j.1574-6941.1999.tb00648.x
83. Gião, M. S., Azevedo, N. F., Wilks, S. A., Vieira, M. J., and Keevil, C. W. (2011). Interaction of Legionella pneumophila and Helicobacter pylori with bacterial species isolated from drinking water biofilms. BMC Microbiol. 11:57. doi: 10.1186/1471-2180-11-57
84. Gião, M. S., and Keevil, C. W. (2014). Listeria monocytogenes can form biofilms in tap water and enter into the viable but non-cultivable state. Microb. Ecol. 67, 603-611. doi: 10.1007/s00248-013-0364-3
85. González-Escalona, N., Fey, A., Höfle, M. G., Espejo, R. T., and Guzmán, C. A. (2006). Quantitative reverse transcription polymerase chain reaction analysis of Vibrio cholerae cells entering the viable but non-culturable state and starvation in response to cold shock. Environ. Microbiol. 8, 658-666. doi: 10.1111/j.1462-2920.2005.00943.x
86. Gourmelon, M., Cillard, J., and Pommepuy, M. (1994). Visible light damage to Escherichia coli in seawater: oxidative stress hypothesis. J. Appl. Bacteriol. 77, 105-112. doi: 10.1111/j.1365-2672.1994.tb03051.x
87. Grey, B. E., and Steck, T. R. (2001). The viable but nonculturable state of Ralstonia solanacearum may be involved in long-term survival and plant infection. Appl. Environ. Microbiol. 67, 3866-3872. doi: 10.1128/AEM.67.9.3866-3872.2001
88. Gunasekera, T. S., Sørensen, A., Attfield, P. V., Sørensen, S. J., and Veal, D. A. (2002). Inducible gene expression by nonculturable bacteria in milk after pasteurization. Appl. Environ. Microbiol. 68, 1988-1993. doi: 10.1128/AEM.68.4.1988-1993.2002
89. Gupta, R. K., Srivastava, B. S., and Srivastava, R. (2010). Comparative expression analysis of rpf-like genes of Mycobacterium tuberculosis H37Rv under different physiological stress and growth conditions. Microbiology 156, 2714-2722. doi: 10.1099/mic.0.037622-0
90. Gupte, A. R., de Rezende, C. L. E., and Joseph, S. W. (2003). Induction and resuscitation of viable but nonculturable Salmonella enterica serovar Typhimurium DT104. Appl. Environ. Microbiol. 69, 6669-6675. doi: 10.1128/AEM.69.11.6669-6675.2003
91. Heidelberg, J. F., Shahamat, M., Levin, M., Rahman, I., Stelma, G., Grim, C., et al. (1997). Effect of aerosolization on culturability and viability of gram-negative bacteria. Appl. Environ. Microbiol. 63, 3585-3588.
92. Heim, S., Lleò, M. M., Bonato, B., Guzman, C. A., and Canepari, P. (2002). The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J. Bacteriol. 184, 6739-6745. doi: 10.1128/JB.184.23.6739-6745.2002
93. Helaine, S., and Kugelberg, E. (2014). Bacterial persisters: formation, eradication, and experimental systems. Trends Microbiol. doi: 10.1016/j.tim.2014.03.008. [Epub ahead of print].
94. Hengge-Aronis, R. (1993). Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell 72, 165-168. doi: 10.1016/0092-8674(93)90655-A
95. Hett, E. C., Chao, M. C., Steyn, A. J., Fortune, S. M., Deng, L. L., and Rubin, E. J. (2007). A partner for the resuscitation-promoting factors of Mycobacterium tuberculosis. Mol. Microbiol. 66, 658-668. doi: 10.1111/j.1365-2958.2007.05945.x
96. Hishinuma, S., Yuki, M., Fujimura, M., and Fukumori, F. (2006). OxyR regulated the expression of two major catalases, KatA and KatB, along with peroxiredoxin, AhpC in Pseudomonas putida. Environ. Microbiol. 8, 2115-2124. doi: 10.1111/j.1462-2920.2006.01088.x
97. Hurst, A. (1977). Bacterial injury: a review. Can. J. Microbiol. 23, 935-944. doi: 10.1139/m77-139
98. Igo, M., and Silhavy, T. (1988). EnvZ, a transmembrane environmental sensor of Escherichia coli K-12, is phosphorylated in vitro. J. Bacteriol. 170, 5971-5973.
99. Inglis, T. J. J., and Sagripanti, J.L. (2006). Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl. Environ. Microbiol. 72, 6865-6875. doi: 10.1128/AEM.01036-06
100. Israely, T., Banin, E., and Rosenberg, E. (2001). Growth, differentiation and death of Vibrio shiloi in coral tissue as a function of seawater temperature. Aquat. Microb. Ecol. 24, 1-8. doi: 10.3354/ame024001
101. Jones, T. F., and Gerner-Smidt, P. (2012). Nonculture diagnostic tests for enteric diseases. Emerg. Infect. Dis. 18, 513. doi: 10.3201/eid1803.111914
102. Kana, B. D., Gordhan, B. G., Downing, K. J., Sung, N., Vostroktunova, G., Machowski, E. E., et al. (2008). The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol. Microbiol. 67, 672-684. doi: 10.1111/j.1365-2958.2007.06078.x
103. Kardas, P. (2002). Patient compliance with antibiotic treatment for respiratory tract infections. J. Antimicrob. Chemother. 49, 897-903. doi: 10.1093/jac/dkf046
104. Kell, D. B., and Young, M. (2000). Bacterial dormancy and culturability: the role of autocrine growth factors: commentary. Curr. Opin. Microbiol. 3, 238-243. doi: 10.1016/S1369-5274(00)00082-5
105. Klančnik, A., Guzej, B., Jamnik, P., Vučković, D., Abram, M., and Možina, S. S. (2009). Stress response and pathogenic potential of Campylobacter jejuni cells exposed to starvation. Res. Microbiol. 160, 345-352. doi: 10.1016/j.resmic.2009.05.002
106. Koebnik, R., Locher, K. P., and Van Gelder, P. (2000). Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37, 239-253. doi: 10.1046/j.1365-2958.2000.01983.x
107. Kogure, K., Simidu, U., and Taga, N. (1979). A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25, 415-420. doi: 10.1139/m79-063
108. Koltunov, V., Greenblatt, C., Goncharenko, A., Demina, G., Klein, B., Young, M., et al. (2010). Structural changes and cellular localization of resuscitation-promoting factor in environmental isolates of Micrococcus luteus. Microb. Ecol. 59, 296-310. doi: 10.1007/s00248-009-9573-1
109. Kong, I. S., Bates, T. C., Hülsmann, A., Hassan, H., Smith, B. E., and Oliver, J. D. (2004). Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol. Ecol. 50, 133-142. doi: 10.1016/j.femsec.2004.06.004
110. Kusumoto, A., Asakura, H., and Kawamoto, K. (2012). General stress sigma factor RpoS influences time required to enter the viable but non-culturable state in Salmonella enterica. Microbiol. Immunol. 56, 228-237. doi: 10.1111/j.1348-0421.2012.00428.x
111. Kuznetsov, B. A., Davydova, M. E., Shleeva, M. O., Shleev, S. V., Kaprelyants, A. S., and Yaropolov, A. I. (2004). Electrochemical investigation of the dynamics of Mycobacterium smegmatis cells' transformation to dormant, nonculturable form. Bioelectrochemistry 64, 125-131. doi: 10.1016/j.bioelechem.2004.05.001
112. Lahtinen, S. J., Ahokoski, H., Reinikainen, J. P., Gueimonde, M., Nurmi, J., Ouwehand, A. C., et al. (2008). Degradation of 16S rRNA and attributes of viability of viable but nonculturable probiotic bacteria. Lett. Appl. Microbiol. 46, 693-698. doi: 10.1111/j.1472-765X.2008.02374.x
113. Lai, C.J., Chen, S.Y., Lin, I., Chang, C.H., and Wong, H.C. (2009). Change of protein profiles in the induction of the viable but nonculturable state of Vibrio parahaemolyticus. Int. J. Food Microbiol. 135, 118-124. doi: 10.1016/j.ijfoodmicro.2009.08.023
114. Lange, R., and Hengge-Aronis, R. (1991). Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5, 49-59. doi: 10.1111/j.1365-2958.1991.tb01825.x
115. Lee, D. G., Park, S. J., and Kim, S. J. (2007). Influence of pipe materials and VBNC cells on culturable bacteria in a chlorinated drinking water model system. J. Microbiol. Biotechnol. 17, 1558-1562.
116. Lemke, M. J., and Leff, L. G. (2006). Culturability of stream bacteria assessed at the assemblage and population levels. Microb. Ecol. 51, 365-374. doi: 10.1007/s00248-006-9026-z
117. 2Lr cells in forest soil monitored by polymerase chain reaction and spread plating. FEMS Microbiol. Ecol. 16, 71-82. doi: 10.1111/j.1574-6941.1995.tb00270.x
118. Lindbäck, T., Rottenberg, M. E., Roche, S. M., and Rørvik, L. M. (2010). The ability to enter into an avirulent viable but non-culturable (VBNC) form is widespread among Listeria monocytogenes isolates from salmon, patients and environment. Vet. Res. 41, 08. doi: 10.1051/vetres/2009056
119. 157:H7. Water Res. 44, 711-718. doi: 10.1016/j.watres.2009.10.005
120. Lleò, M. M., Benedetti, D., Tafi, M. C., Signoretto, C., and Canepari, P. (2007a). Inhibition of the resuscitation from the viable but non-culturable state in Enterococcus faecalis. Environ. Microbiol. 9, 2313-2320. doi: 10.1111/j.1462-2920.2007.01345.x
121. Lleò, M. M., Bonato, B., Tafi, M. C., Caburlotto, G., Benedetti, D., and Canepari, P. (2007b). Adhesion to medical device materials and biofilm formation capability of some species of enterococci in different physiological states. FEMS Microbiol. Lett. 274, 232-237. doi: 10.1111/j.1574-6968.2007.00836.x
122. Lleò, M. M., Bonato, B., Tafi, M. C., Signoretto, C., Boaretti, M., and Canepari, P. (2001). Resuscitation rate in different enterococcal species in the viable but non-culturable state. J. Appl. Microbiol. 91, 1095-1102. doi: 10.1046/j.1365-2672.2001.01476.x
123. Lleò, M. M., Pierobon, S., Tafi, M. C., Signoretto, C., and Canepari, P. (2000). mRNA detection by reverse transcription-PCR for monitoring viability over time in an Enterococcus faecalis viable but nonculturable population maintained in a laboratory microcosm. Appl. Environ. Microbiol. 66, 4564-4567. doi: 10.1128/AEM.66.10.4564-4567.2000
124. Lleò, M. M., Tafi, M. C., and Canepari, P. (1998). Nonculturable Enterococcus faecalis cells are metabolically active and capable of resuming active growth. Syst. Appl. Microbiol. 21, 333-339. doi: 10.1016/S0723-2020(98)80041-6
125. Longkumer, T., Parthasarathy, S., Vemuri, S. G., and Siddavattam, D. (2014). OxyR-dependent expression of a novel glutathione S-transferase (Abgst01) gene in Acinetobacter baumannii DS002 and its role in biotransformation of organophosphate insecticides. Microbiology 160, 102-112. doi: 10.1099/mic.0.070664-0
126. Maalej, S., Denis, M., and Dukan, S. (2004). Temperature and growth-phase effects on Aeromonas hydrophila survival in natural seawater microcosms: role of protein synthesis and nucleic acid content on viable but temporarily nonculturable response. Microbiology 150, 181-187. doi: 10.1099/mic.0.26639-0
127. Magariños, B., Romalde, J. L., Barja, J. L., and Toranzo, A. E. (1994). Evidence of a dormant but infective state of the fish pathogen Pasteurella piscicida in seawater and sediment. Appl. Environ. Microbiol. 60, 180-186.
128. 157:H7 enter the viable but nonculturable state in salted salmon roe? Appl. Environ. Microbiol. 66, 5536-5539. doi: 10.1128/AEM.66.12.5536-5539.2000
129. Manina, G., and McKinney, J. D. (2013). A single-cell perspective on non-growing but metabolically active (NGMA) bacteria. Curr. Top. Microbiol. Immunol. 374, 135-161. doi: 10.1007/82_2013_333
130. Marrs, K. A. (1996). The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Biol. 47, 127-158. doi: 10.1146/annurev.arplant.47.1.127
131. Mascher, F., Hase, C., Moënne-Loccoz, Y., and Défago, G. (2000). The viable-but-nonculturable state induced by abiotic stress in the biocontrol agent Pseudomonas fluorescens CHA0 does not promote strain persistence in soil. Appl. Environ. Microbiol. 66, 1662-1667. doi: 10.1128/AEM.66.4.1662-1667.2000
132. Masuda, Y., Tajima, K., and Ezura, Y. (2004). Resuscitation of Tenacibaculum sp., the causative bacterium of spotting disease of sea urchin Strongylocentroutus intermedius, from the viable but non-culturable state. Fisheries Sci. 70, 277-284. doi: 10.1111/j.1444-2906.2003.00801.x
133. McDougald, D., Rice, S. A., and Kjelleberg, S. (2001). SmcR-dependent regulation of adaptive phenotypes in Vibrio vulnificus. J. Bacteriol. 183, 758-762. doi: 10.1128/JB.183.2.758-762.2001
134. Mir, M., Asong, J., Li, X., Cardot, J., Boons, G.J., and Husson, R. N. (2011). The extracytoplasmic domain of the Mycobacterium tuberculosis Ser/Thr kinase PknB binds specific muropeptides and is required for PknB localization. PLoS Path. 7:e1002182. doi: 10.1371/journal.ppat.1002182
135. Misra, R., and Reeves, P. (1987). Role of micF in the tolC-mediated regulation of OmpF, a major outer membrane protein of Escherichia coli K-12. J. Bacteriol. 169, 4722-4730.
136. 2-degrading compounds. Arch. Microbiol. 172, 63-67. doi: 10.1007/s002030050741
137. Muela, A., Seco, C., Camafeita, E., Arana, I., Orruño, M., López, J. A., et al. (2008). Changes in Escherichia coli outer membrane subproteome under environmental conditions inducing the viable but nonculturable state. FEMS Microbiol. Ecol. 64, 28-36. doi: 10.1111/j.1574-6941.2008.00453.x
138. Mukamolova, G. V., Kaprelyants, A. S., Young, D. I., Young, M., and Kell, D. B. (1998a). A bacterial cytokine. Proc. Natl. Acad. Sci. U.S.A. 95, 8916-8921. doi: 10.1073/pnas.95.15.8916
139. Mukamolova, G. V., Murzin, A. G., Salina, E. G., Demina, G. R., Kell, D. B., Kaprelyants, A. S., et al. (2006). Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol. Microbiol. 59, 84-98. doi: 10.1111/j.1365-2958.2005.04930.x
140. Mukamolova, G. V., Turapov, O. A., Malkin, J., Woltmann, G., and Barer, M. R. (2010). Resuscitation-promoting factors reveal an occult population of tubercle bacilli in sputum. Am. J. Respir. Crit. Care Med. 181, 174-180. doi: 10.1164/rccm.200905-0661OC
141. Mukamolova, G. V., Turapov, O. A., Young, D. I., Kaprelyants, A. S., Kell, D. B., and Young, M. (2002). A family of autocrine growth factors in Mycobacterium tuberculosis. Mol. Microbiol. 46, 623-635. doi: 10.1046/j.1365-2958.2002.03184.x
142. Mukamolova, G. V., Yanopolskaya, N. D., Kell, D. B., and Kaprelyants, A. S. (1998b). On resuscitation from the dormant state of Micrococcus luteus. Antonie Van Leeuwenhoek 73, 237-243. doi: 10.1023/A:1000881918216
143. Mulcahy, L. R., Isabella, V. M., and Lewis, K. (2013). Pseudomonas aeruginosa biofilms in disease. Microb. Ecol. doi: 10.1007/s00248-013-0297-x. [Epub ahead of print].
144. Newell, D. G., and Fearnley, C. (2003). Sources of Campylobacter colonization in broiler chickens. Appl. Environ. Microbiol. 69, 4343-4351. doi: 10.1128/AEM.69.8.4343-4351.2003
145. Nguyen, D., Joshi-Datar, A., Lepine, F., Bauerle, E., Olakanmi, O., Beer, K., et al. (2011). Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334, 982-986. doi: 10.1126/science.1211037
146. Nikaido, H., and Vaara, M. (1985). Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49, 1.
147. Nikitushkin, V., Demina, G., Shleeva, M., and Kaprelyants, A. (2013). Peptidoglycan fragments stimulate resuscitation of "non-culturable" mycobacteria. Antonie Van Leeuwenhoek 103, 37-46. doi: 10.1007/s10482-012-9784-1
148. Nilsson, L., Oliver, J. D., and Kjelleberg, S. (1991). Resuscitation of Vibrio vulnificus from the viable but nonculturable state. J. Bacteriol. 173, 5054-5059.
149. Nowakowska, J., and Oliver, J. D. (2013). Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS Microbiol. Ecol. 84, 213-222. doi: 10.1111/1574-6941.12052
150. Nyström, T. (2003). Nonculturable bacteria: programmed survival forms or cells at death's door? Bioessays 25, 204-211. doi: 10.1002/bies.10233
151. O'Toole, G., Kaplan, H. B., and Kolter, R. (2000). Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49-79.
152. Oliver, J. D. (1995). The viable but non-culturable state in the human pathogen Vibrio vulnificus. FEMS Microbiol. Lett. 133, 203-208. doi: 10.1111/j.1574-6968.1995.tb07885.x
153. Oliver, J. D. (2000). "The public health significance of viable but nonculturable bacteria," in Nonculturable Microorganisms in the Environment, eds R. R. Colwell and D. J. Grimes (Washington, DC: ASM press), 277-300.
154. Oliver, J. D. (2005). The viable but nonculturable state in bacteria. J. Microbiol. 43, 93-100.
155. Oliver, J. D., Dagher, M., and Linden, K. (2005). Induction of Escherichia coli and Salmonella typhimurium into the viable but nonculturable state following chlorination of wastewater. J. Water Health 3, 249-257.
156. Oliver, J. D. (2010). Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 34, 415-425. doi: 10.1111/j.1574-6976.2009.00200.x
157. Oliver, J. D., and Bockian, R. (1995). In vivo resuscitation, and virulence towards mice, of viable but nonculturable cells of Vibrio vulnificus. Appl. Environ. Microbiol. 61, 2620-2623.
158. Oliver, J. D., Hite, F., McDougald, D., Andon, N. L., and Simpson, L. M. (1995). Entry into, and resuscitation from, the viable but nonculturable state by Vibrio vulnificus in an estuarine environment. Appl Environ. Microbiol. 61, 2624-2630.
159. Özkanca, R., and Flint, K. (2002). The effect of starvation stress on the porin protein expression of Escherichia coli in lake water. Lett. Appl. Microbiol. 35, 533-537. doi: 10.1046/j.1472-765X.2002.01230.x
160. Ozkanca, R., Sahin, N., Isik, K., Kariptas, E., and Flint, K. (2002). The effect of toluidine blue on the survival, dormancy and outer membrane porin proteins (OmpC and OmpF) of Salmonella typhimurium LT2 in seawater. J. Appl. Microbiol. 92, 1097-1104. doi: 10.1046/j.1365-2672.2002.01642.x
161. Pace, N. R. (2009). Mapping the tree of life: progress and prospects. Microb. Mol. Biol. Rev. 73, 565-576. doi: 10.1128/MMBR.00033-09
162. Pai, S. R., Actor, J. K., Sepulveda, E., Hunter, R. L. Jr., and Jagannath, C. (2000). Identification of viable and non-viable Mycobacterium tuberculosis in mouse organs by directed RT-PCR for antigen 85B mRNA. Microb. Path. 28, 335-342. doi: 10.1006/mpat.2000.0353
163. Panutdaporn, N., Kawamoto, K., Asakura, H., and Makino, S. I. (2006). Resuscitation of the viable but non-culturable state of Salmonella enterica serovar Oranienburg by recombinant resuscitation-promoting factor derived from Salmonella Typhimurium strain LT2. Int. J. Food Microbiol. 106, 241-247. doi: 10.1016/j.ijfoodmicro.2005.06.022
164. Pasquaroli, S., Zandri, G., Vignaroli, C., Vuotto, C., Donelli, G., and Biavasco, F. (2013). Antibiotic pressure can induce the viable but non-culturable state in Staphylococcus aureus growing in biofilms. J. Antimicrob. Chemother. 68, 1812-1817. doi: 10.1093/jac/dkt086
165. Patrone, V., Campana, R., Vallorani, L., Dominici, S., Federici, S., Casadei, L., et al. (2013). CadF expression in Campylobacter jejuni strains incubated under low-temperature water microcosm conditions which induce the viable but non-culturable (VBNC) state. Antonie van Leeuwenhoek 103, 979-988. doi: 10.1007/s10482-013-9877-5
166. Pawlowski, D. R., Metzger, D. J., Raslawsky, A., Howlett, A., Siebert, G., Karalus, R. J., et al. (2011). Entry of Yersinia pestis into the viable but nonculturable state in a low-temperature tap water microcosm. PLoS ONE 6:e17585. doi: 10.1371/journal.pone.0017585
167. Pinto, D., Almeida, V., Almeida Santos M., and Chambel, L. (2011). Resuscitation of Escherichia coli VBNC cells depends on a variety of environmental or chemical stimuli. J. Appl. Microbiol. 110, 1601-1611. doi: 10.1111/j.1365-2672.2011.05016.x
168. Pinto, D., Santos, M. A., and Chambel, L. (2013). Thirty years of viable but nonculturable state research: unsolved molecular mechanisms. Crit. Rev. Microbiol. doi: 10.3109/1040841X.2013.794127. [Epub ahead of print].
169. Postgate, J. R. (1976). "Death in microbes and macrobes," in The Survival of Vegetative Microbes, eds T. R. G. Gray, and J. R. Postgate (Cambridge: Cambridge University Press), 1-19.
170. Potrykus, K., and Cashel, M. (2008). (p)ppGpp: still magical? Annu. Rev. Microbiol. 62, 35-51. doi: 10.1146/annurev.micro.62.081307.162903
171. Pruzzo, C., Tarsi, R., Lleò, M. M., Signoretto, C., Zampini, M., Pane, L., et al. (2003). Persistence of adhesive properties in Vibrio cholerae after long-term exposure to sea water. Environ. Microbiol. 5, 850-858. doi: 10.1046/j.1462-2920.2003.00498.x
172. Quirós, C., Herrero, M., García, L. A., and Díaz, M. (2009). Quantitative approach to determining the contribution of viable-but-nonculturable subpopulations to malolactic fermentation processes. Appl. Environ. Microbiol. 75, 2977-2981. doi: 10.1128/AEM.01707-08
173. Rahman, I., Shahamat, M., Kirchman, P. A., Russek-Cohen, E., and Colwell, R. R. (1994). Methionine uptake and cytopathogenicity of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 60, 3573-3578.
174. Rahman, M. H., Suzuki, S., and Kawai, K. (2001). Formation of viable but non-culturable state (VBNC) of Aeromonas hydrophila and its virulence in goldfish, Carassius auratus. Microbiol. Res. 156, 103-106. doi: 10.1078/0944-5013-00084
175. Rangel, D. E. (2011). Stress induced cross-protection against environmental challenges on prokaryotic and eukaryotic microbes. World J. Microbiol. Biotechnol. 27, 1281-1296. doi: 10.1007/s11274-010-0584-3
176. Reece, S. T., and Kaufmann, S. H. E. (2012). Floating between the poles of pathology and protection: can we pin down the granuloma in tuberculosis? Curr. Opin. Microbiol. 15, 63-70. doi: 10.1016/j.mib.2011.10.006
177. Reissbrodt, R., Rienaecker, I., Romanova, J. M., Freestone, P. P. E., Haigh, R. D., Lyte, M., et al. (2002). Resuscitation of Salmonella enterica serovar Typhimurium and enterohemorrhagic Escherichia coli from the viable but nonculturable state by heat-stable enterobacterial autoinducer. Appl. Environ. Microbiol. 68, 4788-4794. doi: 10.1128/AEM.68.10.4788-4794.2002
178. Rice, S. A., McDougald, D., and Kjelleberg, S. (2000). Vibrio vulnificus: a physiological and genetic approach to the viable but nonculturable response. J. Infect. Chemother. 6, 115-120. doi: 10.1007/PL00012150
179. Rivers, B., and Steck, T. R. (2001). Viable but nonculturable uropathogenic bacteria are present in the mouse urinary tract following urinary tract infection and antibiotic therapy. Urol. Res. 29, 60-66. doi: 10.1007/s002400000151
180. Roszak, D. B., Grimes, D. J., and Colwell, R. R. (1984). Viable but nonrecoverable stage of Salmonella enteritidis in aquatic systems. Can. J. Microbiol. 30, 334-338. doi: 10.1139/m84-049
181. Rowan, N. J. (2004). Viable but non-culturable forms of food and waterborne bacteria: quo vadis? Trends Food Sci. Technol. 15, 462-467. doi: 10.1016/j.tifs.2004.02.009
182. Rowe, M. T., Dunstall, G., Kirk, R., Loughney, C. F., Cooke, J. L., and Brown, S. R. (1998). Development of an image system for the study of viable but non-culturable forms of Campylobacter jejuni and its use to determine their resistance to disinfectants. Food Microbiol. 15, 491-498. doi: 10.1006/fmic.1997.0178
183. Russo, F. D., and Silhavy, T. J. (1991). EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J. Mol. Biol. 222, 567-580. doi: 10.1016/0022-2836(91)90497-T
184. Scanga, C. A., Mohan, V. P., Joseph, H., Yu, K., Chan, J., and Flynn, J. L. (1999). Reactivation of latent tuberculosis: variations on the Cornell murine model. Infect. Immun. 67, 4531-4538.
185. Senoh, M., Ghosh-Banerjee, J., Ramamurthy, T., Colwell, R. R., Miyoshi, S.I., Nair, G. B., et al. (2012). Conversion of viable but nonculturable enteric bacteria to culturable by co-culture with eukaryotic cells. Microbiol. Immunol. 56, 342-345. doi: 10.1111/j.1348-0421.2012.00440.x
186. Senoh, M., Ghosh-Banerjee, J., Ramamurthy, T., Hamabata, T., Kurakawa, T., Takeda, M., et al. (2010). Conversion of viable but nonculturable Vibrio cholerae to the culturable state by co-culture with eukaryotic cells. Microbiol. Immunol. 54, 502-507. doi: 10.1111/j.1348-0421.2010.00245.x
187. Shleeva, M., Goncharenko, A., Kudykina, Y., Young, D., Young, M., and Kaprelyants, A. (2013). Cyclic Amp-dependent resuscitation of dormant mycobacteria by exogenous free fatty acids. PLoS ONE 8:e82914. doi: 10.1371/journal.pone.0082914
188. Shleeva, M., Mukamolova, G. V., Young, M., Williams, H. D., and Kaprelyants, A. S. (2004). Formation of 'non-culturable' cells of Mycobacterium smegmatis in stationary phase in response to growth under suboptimal conditions and their Rpf-mediated resuscitation. Microbiology 150, 1687-1697. doi: 10.1099/mic.0.26893-0
189. Signoretto, C., Burlacchini, G., Lleò, M. M., Pruzzo, C., Zampini, M., Pane, L., et al. (2004). Adhesion of Enterococcus faecalis in the nonculturable state to plankton is the main mechanism responsible for persistence of this bacterium in both lake and seawater. Appl. Environ. Microbiol. 70, 6892-6896. doi: 10.1128/AEM.70.11.6892-6896.2004
190. Signoretto, C., Lleò, M. M., Tafi, M. C., and Canepari, P. (2000). Cell wall chemical composition of Enterococcus faecalis in the viable but nonculturable state. Appl. Environ. Microbiol. 66, 1953-1959. doi: 10.1128/AEM.66.5.1953-1959.2000
191. Smith, B., and Oliver, J. D. (2006). 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. 72, 1445-1451. doi: 10.1128/AEM.72.2.1445-1451.2006
192. Sperandio, V., Torres, A. G., Jarvis, B., Nataro, J. P., and Kaper, J. B. (2003). Bacteria-host communication: the language of hormones. Proc. Natl. Acad. Sci. U.S.A. 100, 8951-8956. doi: 10.1073/pnas.1537100100
193. Steinert, M., Emödy, L., Amann, R., and Hacker, J. (1997). Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl. Environ. Microbiol. 63, 2047-2053.
194. Stewart, E. J. (2012). Growing unculturable bacteria. J. Bacteriol. 194, 4151-4160. doi: 10.1128/JB.00345-12
195. Stewart, P. S., and Franklin, M. J. (2008). Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6, 199-210. doi: 10.1038/nrmicro1838
196. Sturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, P., Haddix, P. L., Collins, H. L., Fok, A. K., et al. (1994). Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681. doi: 10.1126/science.8303277
197. Sun, F., Chen, J., Zhong, L., Zhang, X.H., Wang, R., Guo, Q., et al. (2008). Characterization and virulence retention of viable but nonculturable Vibrio harveyi. FEMS Microbiol. Ecol. 64, 37-44. doi: 10.1111/j.1574-6941.2008.00442.x
198. Talaro, K. P., Talaro, A., Delisle, G., and Tomalty, L. (2002). Foundations in Microbiology. Blacklick, OH: McGraw-Hill College.
199. Tao, K., Makino, K., Yonei, S., Nakata, A., and Shinagawa, H. (1991). Purification and characterization of the Escherichia coli OxyR protein, the positive regulator for a hydrogen peroxide-inducible regulon. J. Biochem. 109, 262-266.
200. Telkov, M. V., Demina, G. R., Voloshin, S. A., Salina, E. G., Dudik, T. V., Stekhanova, T. N., et al. (2006). Proteins of the Rpf (resuscitation promoting factor) family are peptidoglycan hydrolases. Biochemistry 71, 414-422. doi: 10.1134/S0006297906040092
201. Thomas, C., Hill, D., and Mabey, M. (2002). Culturability, injury and morphological dynamics of thermophilic Campylobacter spp. within a laboratory-based aquatic model system. J. Appl. Microbiol. 92, 433-442. doi: 10.1046/j.1365-2672.2002.01550.x
202. Trevors, J. (2011). Viable but non-culturable (VBNC) bacteria: gene expression in planktonic and biofilm cells. J. Microbiol. Meth. 86, 266-273. doi: 10.1016/j.mimet.2011.04.018
203. Vergne, I., Chua, J., Singh, S. B., and Deretic, V. (2004). Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20, 367-394. doi: 10.1146/annurev.cellbio.20.010403.114015
204. Via, L. E., Fratti, R. A., McFalone, M., Pagan-Ramos, E., Deretic, D., and Deretic, V. (1998). Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897-905.
205. Vora, G. J., Meador, C. E., Bird, M. M., Bopp, C. A., Andreadis, J. D., and Stenger, D. A. (2005). Microarray-based detection of genetic heterogeneity, antimicrobial resistance, and the viable but nonculturable state in human pathogenic Vibrio spp. Proc. Natl. Acad. Sci. U.S.A. 102, 19109-19114. doi: 10.1073/pnas.0505033102
206. Wai, S. N., Mizunoe, Y., Takade, A., and Yoshida, S.I. (2000). A comparison of solid and liquid media for resuscitation of starvation-and low-temperature-induced nonculturable cells of Aeromonas hydrophila. Arch. Microbiol. 173, 307-310. doi: 10.1007/s002030000142
207. Wang, H.W., Chung, C.H., Ma, T.Y., and Wong, H.C. (2013). Roles of alkyl hydroperoxide reductase subunit C (AhpC) in viable but nonculturable Vibrio parahaemolyticus. App. Environ. Microbiol. 79, 3734-3743. doi: 10.1128/AEM.00560-13
208. Wayne, L. G., and Hayes, L. G. (1996). An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect. Immun. 64, 2062-2069.
209. Wei, Q., le Minh, P. N., Dötsch, A., Hildebrand, F., Panmanee, W., Elfarash, A., et al. (2012). Global regulation of gene expression by OxyR in an important human opportunistic pathogen. Nucleic Acids Res. 40, 4320-4333. doi: 10.1093/nar/gks017
210. Weichart, D., and Kjelleberg, S. (1996). Stress resistance and recovery potential of culturable and viable but nonculturable cells of Vibrio vulnificus. Microbiology 142, 845-853. doi: 10.1099/00221287-142-4-845
211. Weichart, D. H., and Kell, D. B. (2001). Characterization of an autostimulatory substance produced by Escherichia coli. Microbiology 147, 1875-1885.
212. Whitesides, M. D., and Oliver, J. D. (1997). Resuscitation of Vibrio vulnificus from the viable but nonculturable state. Appl. Environ. Microbiol. 63, 1002-1005.
213. Williams, H. R., Macey, B. M., Burnett, L. E., and Burnett, K. G. (2009). Differential localization and bacteriostasis of Vibrio campbellii among tissues of the Eastern oyster, Crassostrea virginica. Dev. Comp. Immunol. 33, 592-600. doi: 10.1016/j.dci.2008.10.008
214. Wingender, J., and Flemming, H. C. (2004). Contamination potential of drinking water distribution network biofilms. Water Sci. Technol. 49, 277-286.
215. Wong, H.C., and Liu, S.H. (2008). Characterization of the low-salinity stress in Vibrio vulnificus. J. Food Protect. 71, 416-419.
216. Wong, H.C., and Wang, P. (2004). Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J. Appl. Microbiol. 96, 359-366. doi: 10.1046/j.1365-2672.2004.02166.x
217. Wong, H.C., Wang, P., Chen, S.Y., and Chiu, S.W. (2004). Resuscitation of viable but non-culturable Vibrio parahaemolyticus in a minimum salt medium. FEMS Microbiol. Lett. 233, 269-275. doi: 10.1111/j.1574-6968.2004.tb09491.x
218. Wood, T. K., Knabel, S. J., and Kwan, B. W. (2013). Bacterial persister cell formation and dormancy. Appl. Environ. Microbiol. 79, 7116-7121. doi: 10.1128/AEM.02636-13
219. Xu, H., Roberts, N., Singleton, F. L., Attwell, R. W., Grimes, D. J., and Colwell, R. R. (1982). Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8, 313-323. doi: 10.1007/BF02010671
220. 157:H7: investigation of specific target genes. J. Appl. Microbiol. 92, 633-640. doi: 10.1046/j.1365-2672.2002.01563.x
221. Zandri, G., Pasquaroli, S., Vignaroli, C., Talevi, S., Manso, E., Donelli, G., et al. (2012). Detection of viable but non-culturable staphylococci in biofilms from central venous catheters negative on standard microbiological assays. Clin. Microbiol. Infect. 18, E259-E261. doi: 10.1111/j.1469-0691.2012.03893.x
222. Zeng, B., Zhao, G., Cao, X., Yang, Z., Wang, C., and Hou, L. (2013). Formation and resuscitation of viable but nonculturable Salmonella typhi. Biomed. Res. Int. 2013, 907170. doi: 10.1155/2013/907170
223. 157:H7 by high pressure CO2 and its characteristics. PLoS ONE 8:e62388. doi: 10.1371/journal.pone.0062388
224. Zimmermann, R., Iturriaga, R., and Becker-Birck, J. (1978). Simultaneous determination of the total number of aquatic bacteria and the number thereof involved in respiration. Appl. Environ. Microbiol. 36, 926-935.