Skip to main content
SpringerLink
Log in

Survival strategies of Escherichia coli and Vibrio spp.: contribution of the viable but nonculturable phenotype to their stress-resistance and persistence in adverse environments

  • REVIEW
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

In their natural ecosystems, bacteria are continuously exposed to changing environmental factors including physicochemical parameters (e.g. temperature, pH, etc.), availability of nutrients as well as interaction(s) with other organisms. To increase their tolerance and survival under adverse conditions, bacteria trigger a number of adaptation mechanisms. One of the well-known adaptation responses of the non-spore-forming bacteria is the acquisition of the viable but non-culturable (VBNC) state. This phenotype is induced by different stress factors (e.g. low temperature) and is characterized by the temporal loss of culturability, which can potentially be restored. Moreover, this response can be combined with the bust and boom strategy, which implies the death of the main population of the stressed cells (or their entry into the VBNC state) upon stress, thus enabling the remaining cells (i.e. residual culturable population) to subsist at the expense of the dead or/and VBNC cells. In this review, we discuss the characteristics of the VBNC state, its biological significance and contribution to bacterial survival.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

(adapted from Arana et al. (2004) A. van Leeuwenhoek 86:189–199, Arana et al. (2007) FEMS Microbiol. Ecol. 62:1–11, Kaberdin et al. (2015) Microb. Ecol. 70:689–700, Parada et al. (2016) Microb. Ecol. 72:549–558, and unpublished results)

Fig. 2

(adapted from Arana et al. (2004) A. van Leeuwenhoek 86:189–190)

Similar content being viewed by others

References

  • Abboudi M, Surget SM, Rontani JF, Sempéré R, Joux F (2008) Physiological alteration of the marine bacterium Vibrio angustum S14 exposed to simulated sunlight during growth. Curr Microbiol 57:412–417. doi:10.1007/s00284-008-9214-9

    Article  CAS  Google Scholar 

  • Abia AL, Ubomba-Jaswa E, Momba MN (2016) Competitive survival of Escherichia coli, Vibrio cholerae, Salmonella typhimurium and Shigella dysenteriae in riverbed sediments. Microb Ecol. doi:10.1007/s00248-016-0784-y

    Google Scholar 

  • Aertsen A, Michiels CW (2004) Stress and how bacteria cope with death and survival. Crit Rev Microbiol 30:263–273. doi:10.1080/10408410490884757

    Article  CAS  Google Scholar 

  • Albertini MC, Accorsi A, Teodori L, Pierfelici L, Uguccioni F, Rocchi MB, Burattini S, Citterio B (2006) Use of multiparameter analysis for Vibrio alginolyticus viable but nonculturable state determination. Cytometry A 69:260–265. doi:10.1002/cyto.a.20263

    Article  Google Scholar 

  • Amel BK, Amine B, Amina B (2008) Survival of Vibrio fluvialis in seawater under starvation. Microbiol Res 163:323–328. doi:10.1016/j.micres.2006.06.006

    Article  CAS  Google Scholar 

  • Arana I, Seco C, Epelde K, Muela A, Fernández-Astorga A, Barcina I (2004) Relationships between Escherichia coli cells and the surrounding medium during survival processes. Antonie Van Leeuwenhoek 86:189–199. doi:10.1023/B:ANTO.0000036146.28808.93

    Article  CAS  Google Scholar 

  • Arana I, Orruño M, Pérez-Pascual D, Seco C, Muela A, Barcina I (2007) Inability of Escherichia coli to resuscitate from the viable but nonculturable state. FEMS Microbiol Ecol 62:1–11. doi:10.1111/j.1574-6941.2007.00362.x

    Article  CAS  Google Scholar 

  • Arana I, Muela A, Orruño M, Seco C, Garaizabal I, Barcina I (2010) Effect of temperature and starvation upon survival strategies of Pseudomonas fluorescens CHA0: comparison with Escherichia coli. FEMS Microbiol Ecol 74:500–509. doi:10.1111/j.1574-6941.2010.00979.x

    Article  CAS  Google Scholar 

  • Armada SP, Farto R, Pérez MJ, Nieto TP (2003) Effect of temperature, salinity and nutrient content on the survival responses of Vibrio splendidus biotype I. Microbiology 149:369–375. doi:10.1099/mic.0.25574-0

    Article  CAS  Google Scholar 

  • Asakura H, Ishiwa A, Arakawa E, Makino S, Okada Y, Yamamoto S, Igimi S (2007) 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

    Article  CAS  Google Scholar 

  • Banin E, Vassilakos D, Orr E, Martinez J, Rosenberg E (2003) Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi. Curr Microbiol 46:418–422. doi:10.1007/s00284-002-3912-5

    Article  CAS  Google Scholar 

  • Barcina I, Arana I (2009) The viable but nonculturable phenotype, a crossroad in the live cycle of non differentiating bacteria? Rev Environ Sci BioTechnol 8:245–255. doi:10.1007/s11157-009-9159-x

    Article  Google Scholar 

  • Barria C, Malecki M, Arraiano CM (2013) Bacterial adaptation to cold. Microbiology 159:2437–2443. doi:10.1099/mic.0.052209-0

    Article  CAS  Google Scholar 

  • Bogosian G, Bourneuf EV (2001) A matter of bacterial life and death. EMBO Rep 2:770–774. doi:10.1093/embo-reports/kve182

    Article  CAS  Google Scholar 

  • Chandran A, Mohamed Hatha AA (2005) Relative survival of Escherichia coli and Salmonella typhimurium in a tropical estuary. Water Res 39:1397–1403. doi:10.1016/j.watres.2005.01.010

    Article  CAS  Google Scholar 

  • Colwell RR, Gray DJ (2000) Nonculturable microorganisms in the environment. ASM Press, Washington

    Book  Google Scholar 

  • Coutard F, Crassous P, Droguet M, Gobin E, Colwell RR, Pommepuy M, Hervio-Heath D (2007) Recovery in culture of viable but nonculturable Vibrio parahaemolyticus: regrowth or resuscitation? ISME J 1:111–120. doi:10.1038/ismej.2007.1

    Article  CAS  Google Scholar 

  • Deller S, Mascher F, Platzer S, Reinthaler FF, Marth E (2006) Effect of solar radiation on survival of indicator bacteria in bathing waters. Cent Eur J Public Health 14:133–137

    Google Scholar 

  • Du M, Chen J, Zhang X, Li A, Li Y (2007) Characterization and resuscitation of viable but nonculturable Vibrio alginolyticus VIB283. Arch Microbiol 188:283–288. doi:10.1007/s00203-007-0246-5

    Article  CAS  Google Scholar 

  • Falcioni T, Papa S, Campana R, Manti A, Battistelli M, Baffone W (2008) State transitions of Vibrio parahaemolyticus VBNC cells evaluated by flow cytometry. Cytometry B Clin Cytom 74:272–281. doi:10.1002/cyto.b.20427

    Article  Google Scholar 

  • Hernroth B, Lothigius A, Bölin I (2010) Factors influencing survival of enterotoxigenic Escherichia coli, Salmonella enterica (serovar Typhimurium) and Vibrio parahaemolyticus in marine environments. FEMS Microbiol Ecol 71:272–280. doi:10.1111/j.1574-6941.2009.00803.x

    Article  CAS  Google Scholar 

  • Imamura D, Mizuno T, Miyoshi S, Shinoda S (2015) Stepwise changes in viable but nonculturable Vibrio cholerae cells. Microbiol Immunol 59:305–310. doi:10.1111/1348-0421.12246

    Article  CAS  Google Scholar 

  • Jia J, Li Z, Cao J, Jiang Y, Liang C, Liu M (2013) Proteomic analysis of protein expression in the induction of the viable but nonculturable state of Vibrio harveyi SF1. Curr Microbiol 67:442–447. doi:10.1007/s00284-013-0383-9

    Article  CAS  Google Scholar 

  • Jiang XP, Chai JT (1996) Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl Environ Microbiol 62:1300–1305

    CAS  Google Scholar 

  • Kaberdin VR, Montánchez I, Parada C, Orruño M, Arana I, Barcina I (2015) Unveiling the metabolic pathways associated with the adaptive reduction of cell size during Vibrio harveyi persistence in seawater microcosms. Microb Ecol 70:689–700. doi:10.1007/s00248-015-0614-7

    Article  CAS  Google Scholar 

  • Kehoe SC, Barer MR, Devlin LO, McGuigan KG (2004) Batch process solar disinfection is an efficient means of disinfecting drinking water contaminated with Shigella dysenteriae type I. Lett Appl Microbiol 38:410–414. doi:10.1111/j.1472-765X.2004.01515.x

    Article  CAS  Google Scholar 

  • Koch AL (1971) The adaptive responses of Escherichia coli to a famine and feast existence. Adv Microb Physiol 6:147–217

    Article  CAS  Google Scholar 

  • Kong IS, Bates TC, Hülsmann 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. doi:10.1016/j.femsec.2004.06.004

    Article  CAS  Google Scholar 

  • Korajkic A, Wanjugi P, Harwood VJ (2013) Indigenous microbiota and habitat influence Escherichia coli survival more than sunlight in simulated aquatic environments. Appl Environ Microbiol 79:5329–5337. doi:10.1128/AEM.01362-13

    Article  CAS  Google Scholar 

  • Krebs SJ, Taylor RK (2011) Nutrient-dependent, rapid transition of Vibrio cholerae to coccoid morphology and expression of the toxin co-regulated pilus in this form. Microbiology 157:2942–2953. doi:10.1099/mic.0.048561-0

    Article  CAS  Google Scholar 

  • Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130. doi:10.1038/nrmicro2504

    Article  CAS  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278. doi:10.1146/annurev.physiol.68.040104.110001

    Article  CAS  Google Scholar 

  • Li L, Mendis N, Trigui H, Oliver JD, Faucher SP (2014) The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol 5:258. doi:10.3389/fmicb.2014.00258

    Google Scholar 

  • Liu Y, Wang C, Tyrrell G, Hrudey SE, Li XF (2009) Induction of Escherichia coli O157:H7 into the viable but non-culturable state by chloraminated water and river water, and subsequent resuscitation. Environ Microbiol Rep 1:155–161. doi:10.1111/j.1758-2229.2009.00024.x

    Article  CAS  Google Scholar 

  • Lothigius A, Sjöling A, Svennerholm AM, Bölin I (2010) Survival and gene expression of enterotoxigenic Escherichia coli during long-term incubation in sea water and freshwater. J Appl Microbiol 108:1441–1449. doi:10.1111/j.1365-2672.2009.04548.x

    Article  CAS  Google Scholar 

  • Makino SI, Kii T, Asakura H, Shirahata T, Ikeda T, Takeshi K, Itoh K (2000) Does enterohemorrhagic Escherichia coli O157:H7 enter the viable but nonculturable state in salted salmon roe? Appl Environ Microbiol 66:5536–5539

    Article  CAS  Google Scholar 

  • Mendis N, McBride P, Faucher SP (2015) Short-term and long-term survival and virulence of Legionella pneumophila in the defined freshwater medium Fraquil. PLoS ONE 10:e0139277. doi:10.1371/journal.pone.0139277

    Article  Google Scholar 

  • Montánchez I, Arana I, Parada C, Garaizabal I, Orruño M, Barcina I, Kaberdin VR (2014) Reprogramming of Vibrio harveyi gene expression during adaptation in cold seawater. FEMS Microbiol Ecol 87:193–203. doi:10.1111/1574-6941.12216

    Article  Google Scholar 

  • Muela A, García-Bringas JM, Seco C, Arana I, Barcina I (2002) Participation of oxygen and role of exogenous and endogenous sensitizers in the photoinactivation of Escherichia coli by photosynthetically active radiation, UV-A and UV-B. Microb Ecol 44:354–364. doi:10.1007/s00248-002-1027-y

    Article  CAS  Google Scholar 

  • Munn CB, Marchant HK, Moody AJ (2008) Defences against oxidative stress in vibrios associated with corals. FEMS Microbiol Lett 281:58–63. doi:10.1111/j.1574-6968.2008.01073.x

    Article  CAS  Google Scholar 

  • Na SH, Miyanaga K, Unno H, Tanji Y (2006) The survival response of Escherichia coli K12 in a natural environment. Appl Microbiol Biotechnol 72:386–392. doi:10.1007/s00253-005-0268-3

    Article  CAS  Google Scholar 

  • Neidhardt FC (1999) Bacterial growth: constant obsession with dN/dt. J Bacteriol 181:7405–7408

    CAS  Google Scholar 

  • Noble RT, Lee IM, Schiff KC (2004) Inactivation of indicator micro-organisms from various sources of faecal contamination in seawater and freshwater. J Appl Microbiol 96:464–472

    Article  CAS  Google Scholar 

  • Nowakowska J, Oliver JD (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

    Article  CAS  Google Scholar 

  • Nyström T (2001) Not quite dead enough: on bacterial life, culturability, senescence, and death. Arch Microbiol 176:159–164

    Article  Google Scholar 

  • Oliver JD (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

    Article  CAS  Google Scholar 

  • Oliver JD (2016) The viable but nonculturable state for bacteria: status update. Microbe 11:159–164

    Google Scholar 

  • Parada C, Orruño M, Kaberdin V, Bravo Z, Barcina I, Arana I (2016) Changes in the Vibrio harveyi cell envelope subproteome during permanence in cold seawater. Microb Ecol 72:549–558. doi:10.1007/s00248-016-0802-0

    Article  CAS  Google Scholar 

  • Pienaar JA, Singh A, Barnard TG (2016) The viable but nonculturable state in pathogenic Escherichia coli: a general review. Afr J Lab Med 5:a368. doi:10.4102/ajlm.v5i1.368

    Article  Google Scholar 

  • Pinto D, Almeida V, Almeida Santos M, 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

    Article  CAS  Google Scholar 

  • Pinto D, Santos MA, Chambel L (2015) Thirty years of viable but nonculturable state research: unsolved molecular mechanisms. Crit Rev Microbiol 41:61–76. doi:10.3109/1040841X.2013.794127

    Article  Google Scholar 

  • Pruzzo C, Tarsi R, Lleo MM, Signoretto C, Zampini M, Pane L, Colwell RR, Canepari P (2003) Persistence of adhesive properties in Vibrio cholerae after long-term exposure to sea water. Environ Microbiol 5:850–858

    Article  CAS  Google Scholar 

  • Ramamurthy T, Ghosh A, Pazhani GP, Shinoda S (2014) Current perspectives on viable but non-culturable (VBNC) pathogenic bacteria. Front. Public Health 2:103. doi:10.3389/fpubh.2014.00103

    Google Scholar 

  • Ramos JL, Gallegos MT, Marqués S, Ramos-González MI, Espinosa-Urgel M, Segura A (2001) Responses of Gram-negative bacteria to certain environmental stressors. Curr Opin Microbiol 4:166–171

    Article  CAS  Google Scholar 

  • Rao NV, Shashidhar R, Bandekar JR (2014) Induction, resuscitation and quantitative real-time polymerase chain reaction analyses of viable but nonculturable Vibrio vulnificus in artificial sea water. World J Microbiol Biotechnol 30:2205–2212. doi:10.1007/s11274-014-1640-1

    Article  CAS  Google Scholar 

  • Rittershaus ESC, Baek SH, Sassetti CM (2013) The normalcy of dormancy: common themes in microbial quiescence. Cell Host Microbe 13:643–651. doi:10.1016/j.chom.2013.05.012

    Article  CAS  Google Scholar 

  • Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51:365–379

    CAS  Google Scholar 

  • Rowan NJ (2004) Viable but non-culturable forms of food and waterborne bacteria: quo vadis? Trends Food Sci Tech 15:462–467. doi:10.1016/j.tifs.2004.02.009

    Article  CAS  Google Scholar 

  • Ruiz P, Poblete-Morales M, Irgang R, Toranzo AE, Avendaño-Herrera R (2016) Survival behaviour and virulence of the fish pathogen Vibrio ordalii in seawater microcosms. Dis Aquat Organ 120:27–38. doi:10.3354/dao03005

    Article  Google Scholar 

  • Sampson RW, Swiatnicki SA, Osinga VL, Supita JL, McDermott CM, Kleinheinz GT (2006) Effects of temperature and sand on E. coli survival in a northern lake water microcosm. J Water Health 4:389–393

    Article  Google Scholar 

  • Signoretto C, Lleò M, Canepari P (2002) Modification of the peptidoglycan of Escherichia coli in the viable but nonculturable state. Curr Microbiol 44:125–131

    Article  CAS  Google Scholar 

  • Silhan J, Corfitzen CB, Albrechtsen HJ (2006) Effect of temperature and pipe material on biofilm formation and survival of Escherichia coli in used drinking water pipes: a laboratory-based study. Water Sci Technol 54:49–56

    Article  CAS  Google Scholar 

  • 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. doi:10.1128/AEM.72.2.1445-1451.2006

    Article  CAS  Google Scholar 

  • Su X, Guo L, Ding L, Qu K, Shen C (2016) Induction of viable but nonculturable state in Rhodococcus and transcriptome analysis using RNA-sEq. PLoS One 11:e0147593. doi:10.1371/journal.pone.0147593

    Article  Google Scholar 

  • Sun F, Chen J, Zhong L, Zhang X-h, Wang R, Guo Q, Dong Y (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

    Article  CAS  Google Scholar 

  • Tarr CL, Patel JS, Puhr ND, Sowers EG, Bopp CA, Strockbine NA (2007) Identification of Vibrio isolates by a multiplex PCR assay and rpoB sequence determination. J Clin Microbiol 45:134–140. doi:10.1128/JCM.01544-06

    Article  CAS  Google Scholar 

  • Thompson CC, Vicente AC, Souza RC, Vasconcelos AT, Vesth T, Alves N Jr, Ussery DW, Iida T, Thompson FL (2009) Genomic taxonomy of Vibrios. BMC Evol Biol 9:258. doi:10.1186/1471-2148-9-258

    Article  Google Scholar 

  • van Elsas JD, Semenov AV, Costa R, Trevors JT (2011) Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME 5:173–183. doi:10.1038/ismej.2010.80.

    Article  Google Scholar 

  • Vattakaven T, Bond P, Bradley G, Munn CB (2006) Differential effects of temperature and starvation on induction of the viable-but-nonculturable state in the coral pathogens Vibrio shiloi and Vibrio tasmaniensis. Appl Environ Microbiol 72:6508–6513. doi:10.1128/AEM.00798-06

    Article  CAS  Google Scholar 

  • Xu HS, Roberts N, Singleton FL, Attwell RW, Grimes DJ, Colwell RR (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

    Article  CAS  Google Scholar 

  • Zhao F, Bi X, Hao Y, Liao X (2013) Induction of viable but nonculturable Escherichia coli O157:H7 by high pressure CO2 and its characteristics. PLoS ONE 8:e62388. doi: 10.1371/journal.pone.0062388

    Article  CAS  Google Scholar 

  • Zhong L, Chen J, Zhang XH, Jiang YA (2009) Entry of Vibrio cincinnatiensis into viable but nonculturable state and its resuscitation. Lett Appl Microbiol 48:247–252. doi:10.1111/j.1472-765X.2008.02522.x

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Immunology, Microbiology and Parasitology, University of the Basque Country (UPV/EHU), Barrio Sarriena S/n, 48940, Leioa, Spain

    M. Orruño, V. R. Kaberdin & I. Arana

  2. IKERBASQUE, Basque Foundation for Science, María Díaz de Haro 3, 48013, Bilbao, Spain

    V. R. Kaberdin

Authors
  1. M. Orruño
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. R. Kaberdin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Arana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Arana.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orruño, M., Kaberdin, V.R. & Arana, I. Survival strategies of Escherichia coli and Vibrio spp.: contribution of the viable but nonculturable phenotype to their stress-resistance and persistence in adverse environments. World J Microbiol Biotechnol 33, 45 (2017). https://doi.org/10.1007/s11274-017-2218-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-017-2218-5

Keywords

Search

Navigation