Interspecific quorum sensing mediates the resuscitation of viable but nonculturable vibrios

Applied and Environmental Microbiology

Volumn 80, Issue 8, 2014, Pages 2478-2483

  Ayrapetyan, Mesrop ^a   Williams, Tiffany C ^a   Oliver, James D ^a,b  

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

^b DUKE UNIVERSITY MARINE LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; MICROBIOLOGY; RESUSCITATION; SEAWATER EFFECTS;

HARSH ENVIRONMENT; MICROBIAL ECOLOGY; MOLECULAR MECHANISM; QUORUM-SENSING INHIBITORS; SUITABLE CONDITIONS; SURVIVAL MECHANISMS; VIABLE BUT NON-CULTURABLE; VIBRIO VULNIFICUS;

BACTERIA;

ALDEHYDE; DORMANCY; HEALTH IMPACT; INTERSPECIFIC COMPETITION; MICROBIAL ACTIVITY; PUBLIC HEALTH; SURVIVAL;

HOMOSERINE; LACTONE; N-OCTANOYLHOMOSERINE LACTONE; SEA WATER;

ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; OYSTER; PHYSIOLOGY; QUORUM SENSING; VIBRIO VULNIFICUS;

ANIMALS; HOMOSERINE; LACTONES; MICROBIAL VIABILITY; OSTREIDAE; QUORUM SENSING; SEAWATER; VIBRIO VULNIFICUS;

EID: 84896974251     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00080-14     Document Type: Article

References (45)

1. Pinto D, Santos MA, Chambel L. 12 July 2013. Thirty years of viable but nonculturable state research: unsolved molecular mechanisms. Crit. Rev. Microbiol. http://dx.doi.org/10.3109/1040841X.2013.794127.
2. Oliver JD. 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 34:415-425. http://dx.doi.org/10.1111/j.1574-6976.2009.00200.x.
3. Oliver JD. 2005. The viable but nonculturable state in bacteria. J. Microbiol. 43:93-100. http://www.ncbi.nlm.nih.gov/pubmed/15765062.
4. Nowakowska J, Oliver JD. 2013. Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS Microbiol. Ecol. 84:213-222. http://dx.doi.org/10.1111/1574-6941.12052.
5. Oliver JD, Bockian R. 1995. In vivo resuscitation, and virulence towards mice, of viable but nonculturable cells of Vibrio vulnificus. Appl. Environ. Microbiol. 61:2620-2623.
6. Kaspar CW, Tamplin ML. 1993. Effects of temperature and salinity on the survival of Vibrio vulnificus in seawater and shellfish. Appl. Environ. Microbiol. 59:2425-2429.
7. Oliver JD, Kaper JB. 2001. Vibrio species, p 263-300. In Doyle MP, Beuchat LR, Montville TJ (ed), Food microbiology: fundamentals and frontiers. American Society for Microbiology, Washington, DC.
8. CDC. 2007. Summary of human Vibrio cases reported to CDC. Centers for Disease Control and Prevention, Atlanta, GA.
9. Blackwell KD, Oliver JD. 2008. The ecology of Vibrio vulnificus, Vibrio cholerae, and Vibrio parahaemolyticus in North Carolina estuaries. J. Microbiol. 46:146-153. http://dx.doi.org/10.1007/s12275-007-0216-2.
10. Oliver JD, Hite F, McDougald D, Andon NL, Simpson LM. 1995. Entry into, and resuscitation from, the viable but nonculturable state by Vibrio vulnificus in an estuarine environment. Appl. Environ. Microbiol. 61: 2624-2630.
11. Oliver JD. 2006. Vibrio vulnificus, p 349-366. In Thompson FL, Austin B, Swings J (ed), The biology of vibrios. American Society for Microbiology, Washington, DC.
12. Froelich B, Oliver JD. 2013. The interactions of Vibrio vulnificus and the oyster Crassostrea virginica. Microb. Ecol. 65:807-816. http://dx.doi.org/10.1007/s00248-012-0162-3.
13. Oliver JD. 2005. Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiol. Infect. 133:383-391. http://dx.doi.org/10.1017/S0950268805003894.
14. Dechet AM, Yu PA, Koram N, Painter J. 2008. Nonfoodborne Vibrio infections: an important cause of morbidity and mortality in the United States, 1997-2006. Clin. Infect. Dis. 46:970-976. http://dx.doi.org/10.1086/529148.
15. Jones MK, Oliver JD. 2009. Vibrio vulnificus: disease and pathogenesis. Infect. Immun. 77:1723-1733. http://dx.doi.org/10.1128/IAI.01046-08.
16. Oliver JD. 2013. Vibrio vulnificus: death on the half shell. A personal journey with the pathogen and its ecology. Microb. Ecol. 65:793-799. http://dx.doi.org/10.1007/s00248-012-0140-9.
17. Feldhusen F. 2000. The role of seafood in bacterial foodborne diseases. Microb. Infect. Inst. Pasteur 2:1651-1660. http://dx.doi.org/10.1016/S1286-4579(00)01321-6.
18. Whitesides MD, Oliver JD. 1997. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. Appl. Environ. Microbiol. 63:1002-1005.
19. Froelich B, Oliver JD. 2013. Increases of Vibrio spp. in oysters upon addition of exogenous bacteria. Appl. Environ. Microbiol. 79:5208-5213. http://dx.doi.org/10.1128/AEM.01110-13.
20. Bari SM, Roky MK, Mohiuddin M, Kamruzzaman M, Mekalanos JJ, Faruque SM. 2013. Quorum-sensing autoinducers resuscitate dormant Vibrio cholerae in environmental water samples. Proc. Natl. Acad. Sci. U. S. A. 110:9926-9931. http://dx.doi.org/10.1073/pnas.1307697110.
21. Bassler BL. 1999. How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr. Opin. Microbiol. 2:582-587. http://dx.doi.org/10.1016/S1369-5274(99)00025-9.
22. Withers H, Swift S, Williams P. 2001. Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr. Opin. Microbiol. 4:186-193. http://dx.doi.org/10.1016/S1369-5274(00) 00187-9.
23. Antunes LC, Ferreira RB, Buckner MM, Finlay BB. 2010. Quorum sensing in bacterial virulence. Microbiology 156:2271-2282. http://dx.doi.org/10.1099/mic.0.038794-0.
24. McDougald D, Srinivasan S, Rice SA, Kjelleberg S. 2003. Signalmediated cross-talk regulates stress adaptation in Vibrio species. Microbiology 149:1923-1933. http://dx.doi.org/10.1099/mic.0.26321-0.
25. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2:a012427. http://dx.doi.org/10.1101/cshperspect.a012427.
26. Cunningham E, Obyrne C, Oliver JD. 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. http://dx.doi.org/10.1016/j.foodcont.2009.03.005.
27. Beam DM. 2004. The role of AI-2 in Vibrio vulnificus. M.S. thesis. University of North Carolina at Charlotte, Charlotte, NC.
28. Hulsmann A, Rosche TM, Kong IS, Hassan HM, Beam DM, Oliver JD. 2003. RpoS-dependent stress response and exoenzyme production in Vibrio vulnificus. Appl. Environ. Microbiol. 69:6114-6120. http://dx.doi.org/10.1128/AEM.69.10.6114-6120.2003.
29. Greenberg EP, Hastings JW, Ulitzur S. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch. Microbiol. 120:87-91. http://dx.doi.org/10.1007/BF00409093.
30. Williams TC, Froelich B, Oliver JD. 2013. A new culture-based method for the improved identification of Vibrio vulnificus from environmental samples, reducing the need for molecular confirmation. J. Microbiol. Methods 93:277-283. http://dx.doi.org/10.1016/j.mimet.2013.03.023.
31. Tsuchikama K, Lowery CA, Janda KD. 2011. Probing autoinducer-2 based quorum sensing: the biological consequences of molecules unable to traverse equilibrium states. J. Org. Chem. 76:6981-6989. http://dx.doi.org/10.1021/jo200882k.
32. Brackman G, Defoirdt T, Miyamoto C, Bossier P, Van Calenbergh S, Nelis H, Coenye T. 2008. Cinnamaldehyde and cinnamaldehyde derivatives reduce virulence in Vibrio spp. by decreasing the DNA-binding activity of the quorum sensing response regulator LuxR. BMC Microbiol. 8:149. http://dx.doi.org/10.1186/1471-2180-8-149.
33. Bassler BL, Greenberg EP, Stevens AM. 1997. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J. Bacteriol. 179:4043-4045.
34. Kaprelyants AS, Kell DB. 1993. Dormancy in stationary-phase cultures of Micrococcus luteus: flow cytometric analysis of starvation and resuscitation. Appl. Environ. Microbiol. 59:3187-3196.
35. McDougald D, Rice SA, Kjelleberg S. 2000. The marine pathogen Vibrio vulnificus encodes a putative homologue of the Vibrio harveyi regulatory gene, luxR: a genetic and phylogenetic comparison. Gene 248:213-221. http://dx.doi.org/10.1016/S0378-1119(00)00117-7.
36. Buerger S, Spoering A, Gavrish E, Leslin C, Ling L, Epstein SS. 2012. Microbial scout hypothesis, stochastic exit from dormancy, and the nature of slow growers. Appl. Environ. Microbiol. 78:3221-3228. http://dx.doi.org/10.1128/AEM.07307-11.
37. Epstein SS. 2009. Microbial awakenings. Nature 457:1083. http://dx.doi.org/10.1038/4571083a.
38. Kong IS, Bates TC, Hulsmann A, Hassan H, Smith BE, Oliver JD. 2004. Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol. Ecol. 50:133-142. http://dx.doi.org/10.1016/j.femsec.2004.06.004.
39. Smith B, Oliver JD. 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. http://dx.doi.org/10.1128/AEM.72.2.1445-1451.2006.
40. Park KJ, Kang MJ, Kim SH, Lee HJ, Lim JK, Choi SH, Park SJ, Lee KH. 2004. Isolation and characterization of rpoS from a pathogenic bacterium, Vibrio vulnificus: role of sigmaS in survival of exponential-phase cells under oxidative stress. J. Bacteriol. 186:3304-3312. http://dx.doi.org/10.1128/JB.186.11.3304-3312.2004.
41. Boaretti M, Lleo MM, Bonato B, Signoretto C, Canepari P. 2003. Involvement of rpoS in the survival of Escherichia coli in the viable but non-culturable state. Environ. Microbiol. 5:986-996. http://dx.doi.org/10.1046/j.1462-2920.2003.00497.x.
42. Joelsson A, Kan B, Zhu J. 2007. Quorum sensing enhances the stress response in Vibrio cholerae. Appl. Environ. Microbiol. 73:3742-3746. http://dx.doi.org/10.1128/AEM.02804-06.
43. Coutard F, Lozach S, Pommepuy M, 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. http://dx.doi.org/10.1128/AEM.02776-06.
44. Maisonneuve E, Castro-Camargo M, Gerdes K. 2013. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154:1140-1150. http://dx.doi.org/10.1016/j.cell.2013.07.048.
45. Manina G, McKinney JD. 2013. A single-cell perspective on non-growing but metabolically active (NGMA) bacteria. Curr. Top. Microbiol. Immunol. 374:135-161. http://dx.doi.org/10.1007/82_2013_333.