Ocean Warming and Spread of Pathogenic Vibrios in the Aquatic Environment

Abstract

Vibrios are among the most common bacteria that inhabit surface waters throughout the world and are responsible for a number of severe infections both in humans and animals. Several reports recently showed that human Vibrio illnesses are increasing worldwide including fatal acute diarrheal diseases, such as cholera, gastroenteritis, wound infections, and septicemia. Many scientists believe this increase may be associated with global warming and rise in sea surface temperature (SST), although not enough evidence is available to support a causal link between emergence of Vibrio infections and climate warming. The effect of increased SST in promoting spread of vibrios in coastal and brackish waters is considered a causal factor explaining this trend. Field and laboratory studies carried out over the past 40 years supported this hypothesis, clearly showing temperature promotes Vibrio growth and persistence in the aquatic environment. Most recently, a long-term retrospective microbiological study carried out in the coastal waters of the southern North Sea provided the first experimental evidence for a positive and significant relationship between SST and Vibrio occurrence over a multidecadal time scale. As a future challenge, macroecological studies of the effects of ocean warming on Vibrio persistence and spread in the aquatic environment over large spatial and temporal scales would conclusively support evidence acquired to date combined with studies of the impact of global warming on epidemiologically relevant variables, such as host susceptibility and exposure. Assessing a causal link between ongoing climate change and enhanced growth and spread of vibrios and related illness is expected to improve forecast and mitigate future outbreaks associated with these pathogens.

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References

  1. 1.

    IPCC (2007) Climate change 2007: synthesis report. IPCC, Geneva

    Google Scholar 

  2. 2.

    Roemmich D, Gould WJ, Gilson J (2012) 135 years of global ocean warming between the Challenger expedition and the Argo Programme. Nat Clim Change 2:425–428

    Article  Google Scholar 

  3. 3.

    Reid PC, Gorick G, Edwards M (2011) Climate change and European Marine Ecosystem Research. Sir Alister Hardy Foundation for Ocean Science, Plymouth, 53 p

    Google Scholar 

  4. 4.

    Kirov B, Georgieva K (2001) Long-term variations and interrelations of ENSO, NAO and solar activity. Phys Chem Earth 27(6–8):441–448

    Google Scholar 

  5. 5.

    Hakkinen S (2002) Surface salinity variability in the northern North Atlantic during recent decades. J Geophys Res 107:8003

    Article  Google Scholar 

  6. 6.

    Pruzzo C, Huq A, Colwell RR, Donelli G (2005) Pathogenic Vibrio species in the marine and estuarine environment. In: Belkin S, Colwell RR (eds) Ocean and health pathogens in the marine environment. Springer, Heidelberg, pp 217–252

    Chapter  Google Scholar 

  7. 7.

    Oliver JD, Pruzzo C, Vezzulli L, Kaper JB (2013) Vibrio species. In: Doyle MP, Buchanan RL (eds) Food microbiology: fundamentals and frontiers, 4th edn. ASM, Washington, pp 401–440. doi:10.1128/9781555818463.ch16

    Google Scholar 

  8. 8.

    World Health Organization: Cholera, 2010. Weekly Epidemiological Record 2011, 86:325–340

    Google Scholar 

  9. 9.

    Newton A, Kendall M, Vugia DJ, Henao OL, Mahon BE (2012) Increasing rates of vibriosis in the United States, 1996–2010: review of surveillance data from 2 systems. Clin Infect Dis 54(5):391–395

    Article  Google Scholar 

  10. 10.

    González-Escalona N, Cachicas V, Acevedo C, Rioseco ML, Vergara JA, Cabello F et al (2005) Vibrio parahaemolyticus diarrhea, Chile, 1998 and 2004. Emerging Infect Dis 11:129–131

    PubMed  Article  Google Scholar 

  11. 11.

    Martinez-Urtaza J, Huapaya B, Gavilan RG, Blanco-Abad V, Ansede-Bermejo J, Cadarso-Suarez C et al (2008) Emergence of Asiatic Vibrio diseases in South America in phase with El Niño. Epidemiology 19:829–837

    PubMed  Article  Google Scholar 

  12. 12.

    CDC (Centers for Disease Control and Prevention) (2008) Outbreak of Vibrio parahaemolyticus infections associated with eating raw oysters—Pacific Northwest, 1997. Morb Mort Week Rep 47:457–462

    Google Scholar 

  13. 13.

    Paz S, Bisharat N, Paz E, Kidar O, Cohen D (2007) Climate change and the emergence of Vibrio vulnificus disease in Israel. Environ Res 103:390–396

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Baker-Austin C, Stockley L, Rangdale R, Martinez-Urtza J (2010) Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environ Micro Rep 2:7–18

    Article  Google Scholar 

  15. 15.

    Baker-Austin C, Trinanes JA, Taylor NGH, Hartnell R, Siitonen A, Martinez-Urtaza J (2012) Emerging Vibrio risk at high latitudes in response to ocean warming. doi:10.1038/nclimate1628

  16. 16.

    Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3:704

    PubMed  Article  Google Scholar 

  17. 17.

    Fernandez MAL, Bauernfeind A, Jimenez JD, Gil CL, El Omeiri N, Guibert DH et al (2009) Influence of temperature and rainfall on the evolution of cholera epidemics in Lusaka, Zambia, 2003–2006: analysis of a time series. T Roy Soc Trop Med H 103(2):137–143

    Article  Google Scholar 

  18. 18.

    Pascual M, Rodó X, Ellner SP, Colwell RR, Bouma MJ (2000) Cholera dynamics and El Niño-Southern oscillation. Science 289(5485):1766–1769

    PubMed  Article  CAS  Google Scholar 

  19. 19.

    Lobitz B, Beck L, Huq A, Wood B, Fuchs G, Faruque AS et al (2000) Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc Nat Acad Sci USA 97:1438–1443

    PubMed  Article  CAS  Google Scholar 

  20. 20.

    Kushmaro A, Bani E, Loya Y, Stackebrandt E, Rosenberg E (2001) Vibrio shiloi sp nov the causative agent of bleaching of the coral Oculina patagonica. Int J Syst Evol Micro 51:1383–1388

    CAS  Google Scholar 

  21. 21.

    Ben-Haim Y, Thompson FL, Thompson CC, Cnockaert MC, Hoste B, Swings J et al (2003) Vibrio coralliilyticus sp nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int J Syst Evol Micr 53:309–315

    Article  CAS  Google Scholar 

  22. 22.

    Vezzulli L, Previati M, Pruzzo C, Marchese A, Bourne DG, Cerrano C (2010) Vibrio infections triggering mass mortality events in a warming Mediterranean sea. Environ Microbiol 12:2007–2019

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Sugumar G, Nakai T, Hirata Y, Matsubara D, Muroga K (1998) Vibrio splendidus biovar II as the causative agent of bacillary necrosis of Japanese oyster Crassostrea gigas larvae. Dis Aquat Organ 33:111–118

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Garnier M, Labreuche Y, Garcia C, Robert A, Nicolas JL (2007) Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microb Ecol 53:187–196

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Weis KE, Hammond RM, Hutchinson R, Blackmore CG (2011) Vibrio illness in Florida, 1998–2007. Epidemiol Infect 139(4):591–598

    PubMed  Article  CAS  Google Scholar 

  26. 26.

    Shearman RK, Lentz SJ (2012) Long-term sea surface temperature variability along the U.S. East Coast. J Phys Oceanogr 40:1004–1017

    Article  Google Scholar 

  27. 27.

    Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS et al (2002) Ecology—climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Semenza JC, Menne B (2009) Climate change and infectious diseases in Europe. Lancet Infect Dis 9(6):365–375

    PubMed  Article  Google Scholar 

  29. 29.

    Lipp EK, Huq A, Colwell RR (2002) Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev 15:757–770

    PubMed  Article  Google Scholar 

  30. 30.

    Colwell RR (2005) Global microbial ecology of Vibrio cholerae. In: Belkin S, Colwell RR (eds) Ocean and health pathogens in the marine environment. Springer, Heidelberg, pp 297–305

    Chapter  Google Scholar 

  31. 31.

    Singleton FL, Attwell R, Jangi S, Colwell RR (1982) Effects of temperature and salinity on Vibrio cholerae growth. Appl Environ Microb 44(5):1047–1058

    CAS  Google Scholar 

  32. 32.

    Huq A, West PA, Small EB, Huq MI, Colwell RR (1984) Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms. Appl Environ Microbiol 48:420–424

    PubMed  CAS  Google Scholar 

  33. 33.

    Pfeffer CS, Hite MF, Oliver JD (2003) Ecology of Vibrio vulnificus in estuarine waters of eastern North Carolina. Appl Environ Microbiol 69(6):3526–3531

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Huq A, Small EB, West PA, Huq MI, Rahman R, Colwell RR (1983) Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl Environ Microbiol 45:275–283

    PubMed  CAS  Google Scholar 

  35. 35.

    Pruzzo C, Vezzulli L, Colwell RR (2008) Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10(6):1400–1410

    PubMed  Article  CAS  Google Scholar 

  36. 36.

    Vezzulli L, Pruzzo C, Huq A, Colwell RR (2010) Environmental reservoirs of Vibrio cholerae and their role in cholera. Env Microbiol Rep 2:27–33

    Article  Google Scholar 

  37. 37.

    Kirschner AKT, Schlesinger J, Farnleitner AH, Hornek R, Suss B, Golda B et al (2008) Rapid growth of planktonic Vibrio cholerae non-O1/non-O139 strains in a large alkaline lake in Austria: dependence on temperature and dissolved organic carbon quality. Appl Environ Microbiol 74(7):2004–2015

    PubMed  Article  CAS  Google Scholar 

  38. 38.

    Worden AZ, Seidel M, Smriga S, Wick A, Malfatti F, Bartlett D et al (2006) Trophic regulation of Vibrio cholerae in coastal marine waters. Environ Microbiol 8:21–29

    PubMed  Article  CAS  Google Scholar 

  39. 39.

    Jensen MA, Faruque SM, Mekalanos JJ, Levin BR (2006) Modelling the role of bacteriophage in the control of cholera outbreaks. Proc Natl Acad Sci USA 103:4652–4657

    PubMed  Article  CAS  Google Scholar 

  40. 40.

    Huq A, Sack RB, Nizam A, Longini IM, Nair GB, Ali A et al (2005) Critical factors influencing the occurrence of Vibrio cholerae in the environment of Bangladesh. Appl Environ Microbiol 71(8):4645–4654

    PubMed  Article  CAS  Google Scholar 

  41. 41.

    Vezzulli L, Pezzati E, Moreno M, Fabiano M, Pane L, Pruzzo C (2009) Benthic ecology of Vibrio spp. and pathogenic Vibrio species in a coastal Mediterranean environment (La Spezia Gulf, Italy). Microb Ecol 58:808–818

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Martinez-Urtaza J, Blanco-Abad V, Rodriguez-Castro A, Ansede-Bermejo J, Miranda A, Rodriguez-Alvarez MX (2012) Ecological determinants of the occurrence and dynamics of Vibrio parahaemolyticus in offshore areas. ISME J 6(5):994–1006

    PubMed  Article  CAS  Google Scholar 

  43. 43.

    Miles DW, Ross T, Olley J, McMeekin TA (1997) Development and evaluation of a predictive model for the effect of temperature and water activity on the growth rate of Vibrio parahaemolyticus. Int J Food Microbiol 38:133–142

    PubMed  Article  CAS  Google Scholar 

  44. 44.

    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

    PubMed  CAS  Google Scholar 

  45. 45.

    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

    Article  Google Scholar 

  46. 46.

    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(2):111–120

    PubMed  Article  CAS  Google Scholar 

  47. 47.

    Kimes NE, Grim CJ, Johnson WR, Hasan NA, Tall BD, Kothary MH et al (2012) Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J 6:835–846

    PubMed  Article  CAS  Google Scholar 

  48. 48.

    Oh MH, Lee SM, Lee DH, Choi SH (2009) Regulation of the Vibrio vulnificus hupA gene by temperature alteration and cyclic AMP receptor protein and evaluation of its role in virulence. Infect Immun 77(3):1208–1215

    PubMed  Article  CAS  Google Scholar 

  49. 49.

    Mahoney JC, Gerding MJ, Jones SH, Whistler CA (2010) Comparison of the pathogenic potentials of environmental and clinical Vibrio parahaemolyticus strains indicates a role for temperature regulation in virulence. Appl Environ Microbiol 76(22):7459–7465

    PubMed  Article  CAS  Google Scholar 

  50. 50.

    Montilla R, Chowdhury MA, Huq A, Xu B, Colwell RR (1996) Serogroup conversion of Vibrio cholerae non-O1 to Vibrio cholerae O1: effect of growth state of cells, temperature, and salinity. Can J Microbiol 42(1):87–93

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    Schuhmacher DA, Klose KE (1999) Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J Bacteriol 181(5):1508–1514

    PubMed  CAS  Google Scholar 

  52. 52.

    Peterson KM (2002) Expression of Vibrio cholerae virulence genes in response to environmental signals. CIIM 3(2):29–38

    PubMed  CAS  Google Scholar 

  53. 53.

    Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR (1990) Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56(6):1977–1980

    PubMed  CAS  Google Scholar 

  54. 54.

    Nelson EJ, Harris JB, Morris JG Jr, Calderwood SB, Camilli A (2009) Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat Rev Microbiol 7:693–702

    PubMed  Article  CAS  Google Scholar 

  55. 55.

    Colwell RR, Huq A, Islam MS, Aziz KMA, Yunus M, Huda Khan N et al (2003) Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA 100(3):1051–1055

    PubMed  Article  CAS  Google Scholar 

  56. 56.

    Huq A (1984) The role of planktonic copepods in the survival and multiplication of Vibrio cholerae in the aquatic environment. University of Maryland, College Park

    Google Scholar 

  57. 57.

    Stauder M, Vezzulli L, Pezzati E, Repetto B, Pruzzo C (2010) Temperature affects Vibrio cholerae O1 El Tor persistence in the aquatic environment via an enhanced expression of GbpA and MSHA adhesins. Env Microbiol Rep 2:140–144

    Article  CAS  Google Scholar 

  58. 58.

    Chiavelli DA, Marsh JW, Taylor RK (2001) The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67:3220–3225

    PubMed  Article  CAS  Google Scholar 

  59. 59.

    Kirn TJ, Jude BA, Taylor RK (2005) A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438:863–866

    PubMed  Article  CAS  Google Scholar 

  60. 60.

    Beaugrand G, Reid PC, Ibañez F, Alistair Lindley J, Edwards M (2002) Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296(5573):1692–1694

    PubMed  Article  CAS  Google Scholar 

  61. 61.

    Moran XAG, Lopez-Urrutia A, Calvo-Diaz A, Li WKW (2010) Increasing importance of small phytoplankton in a warmer ocean. Global Change Biol 16(3):1137–1144

    Article  Google Scholar 

  62. 62.

    Rawlings TK, Ruiz GM, Colwell RR (2007) Association of Vibrio cholerae serogroups O1 El Tor and O139 Bengal with the copepods Acartia tonsa and Eurytemora affinis. Appl Environ Microbiol 73:7926–7933

    PubMed  Article  CAS  Google Scholar 

  63. 63.

    Hsieh JL, Fries JS, Noble RT (2008) Dynamics and predictive modelling of Vibrio spp. in the Neuse river estuary, North Carolina, USA. Environ Microbiol 10(1):57–64

    PubMed  Google Scholar 

  64. 64.

    Randa MA, Polz MF, Lim E (2004) Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Appl Environ Microbiol 70(9):5469–5476

    PubMed  Article  CAS  Google Scholar 

  65. 65.

    Oberbeckmann S, Fuchs BM, Meiners M, Wichels A, Wiltshire KH, Gerdts G (2012) Seasonal dynamics and modeling of a Vibrio community in coastal waters of the North Sea. Microb Ecol 63(3):543–551

    PubMed  Article  Google Scholar 

  66. 66.

    Thompson JR, Randa MA, Marcelino LA, Tomita-Mitchell A, Lim E, Polz MF (2004) Diversity and dynamics of a North Atlantic coastal Vibrio community. Appl Environ Microbiol 70:4103–4110

    PubMed  Article  CAS  Google Scholar 

  67. 67.

    Colwell RR (2000) Viable but nonculturable bacteria: a survival strategy. J Infect Chemother 6:121–125

    PubMed  Article  CAS  Google Scholar 

  68. 68.

    Martinez-Urtaza J, Bowers JC, Trinanes J, DePaola A (2010) Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses. Food Res Int 43(7):1780–1790

    Article  Google Scholar 

  69. 69.

    De Magny GC, Colwell RR (2009) Cholera and climate: a demonstrated relationship. Trans Am Clin Climatol Assoc 120:119–128

    Google Scholar 

  70. 70.

    Vezzulli L, Brettar I, Pezzati E, Reid PC, Colwell RR, Höfle MG, Pruzzo C (2012) Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME J 6:21–30

    PubMed  Article  Google Scholar 

  71. 71.

    Reid PC, Colebrook JM, Matthews JBL, Aiken J (2003) The continuous plankton recorder: concepts and history, from plankton indicator to undulating recorders. Prog Oceanogr 58:117–173

    Article  Google Scholar 

  72. 72.

    Kirby RR, Beaugrand G, Lindley JA, Richardson AJ, Edwards M, Reid PC (2007) Climate effects and benthic–pelagic coupling in the North Sea. Mar Ecol Prog Ser 330:31–38

    Article  Google Scholar 

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Acknowledgments

Support of the National Institutes of Health (Grant no. 2RO1A1039129-11A2-NIH) and National Oceanic and Atmospheric Administration, Oceans and Human Health Initiative (Grant no. S0660009) is gratefully acknowledged. This work was also supported by the Italian Ministry for Universities and Scientific and Technological Research (PRIN project) and by grants from Genoa University.

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Correspondence to Carla Pruzzo.

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Vezzulli, L., Colwell, R.R. & Pruzzo, C. Ocean Warming and Spread of Pathogenic Vibrios in the Aquatic Environment. Microb Ecol 65, 817–825 (2013). https://doi.org/10.1007/s00248-012-0163-2

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Keywords

  • Vibrio
  • Cholera
  • Ocean Warming
  • Vibrio Species
  • VBNC State