Skip to main content

Advertisement

Log in

Impact of Climate Change on Vibrio vulnificus Abundance and Exposure Risk

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Vibrio species are marine bacteria that occur in estuaries worldwide; many are virulent human pathogens with high levels of antibiotic resistance. The average annual incidence of all Vibrio infections has increased by 41% between 1996 and 2005. V. vulnificus (Vv), a species associated with shellfish and occurring in the US Southeast, has ranges of temperature (16–33 °C) and salinity (5–20 ppt) dependencies for optimal growth. Increased water temperatures caused by atmospheric warming and increased salinity gradients caused by sea level rise raise concerns for the effect of climate change on the geographic range of Vv and the potential for increased exposure risk. This research combined monthly field sampling, laboratory analysis, and modeling to identify the current occurrence of Vv in the Winyah Bay estuary (South Carolina, USA) and assess the possible effects of climate change on future geographic range and exposure risk in the estuary. Vv concentrations ranged from 0 to 58 colony forming units (CFU)/mL, salinities ranged from 0 to 28 ppt, and temperature from 18 to 31 °C. A significant empirical relationship was found between Vv concentration and salinity and temperature that fit well with published optimal ranges for growth for these environmental parameters. These results, when coupled with an existing model of future specific conductance, indicated that sea level rise has a greater impact on exposure risk than temperature increases in the estuary. Risk increased by as much as four times compared to current conditions with the largest temporally widespread increase at the most upriver site where currently there is minimal risk.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allen, D.M., V. Ogburn-Matthews, T. Buck, and E.M. Smith. 2008. Mesozooplankton responses to climate change and variability in a southeastern US estuary (1981-2003). Journal of Coastal Research 10055: 95–110. https://doi.org/10.2112/si55-004.1.

    Article  Google Scholar 

  • Baker-Austin, C., and J.D. Oliver. 2018. Vibrio vulnificus: new insights into a deadly opportunistic pathogen. Environmental Microbiology 20 (2): 423–430. https://doi.org/10.1111/1462-2920.13955.

    Article  Google Scholar 

  • Baker-Austin, C., J.V. McArthur, R.C. Tuckfield, M. Najarro, A.H. Lindell, J. Gooch, and R. Stepanauskas. 2008. Antibiotic resistance in the shellfish pathogen Vibrio parahaemolyticus isolated from the coastal water and sediment of Georgia and South Carolina, USA. Journal of Food Protection 71 (12): 2552–2558. https://doi.org/10.4315/0362-028x-71.12.2552.

    Article  CAS  Google Scholar 

  • Baker-Austin, C., L. Stockley, R. Rangdale, and J. Martinez-Urtaza. 2010. Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environmental Microbiology Reports 2 (1): 7–18. https://doi.org/10.1111/j.1758-2229.2009.00096.x.

    Article  Google Scholar 

  • Baker-Austin, C., J.A. Trinanes, N.G.H. Taylor, R. Hartnell, A. Siitonen, and J. Martinez-Urtaza. 2016. Emerging Vibrio risk at high latitudes in response to ocean warming (vol 3, pg 73, 2013). Nature Climate Change 6 (8): 1. https://doi.org/10.1038/nclimate1628.

    Article  Google Scholar 

  • Baker-Austin, C., J. Trinanes, N. Gonzalez-Escalona, and J. Martinez-Urtaza. 2017. Non-cholera Vibrios: the microbial barometer of climate change. Trends in Microbiology 25 (1): 76–84. https://doi.org/10.1016/j.tim.2016.09.008.

    Article  CAS  Google Scholar 

  • Blood, E. R., and F. J. Vernberg. 1992. Characterization of the physical, chemical, and biological conditions and trends in three South Carolina Estuaries: 1970–1985. Volume II – Winyah Bay and North Inlet Estuaries. Charleston, SC.

  • CDC. 2016. Foodborne Diseases Active Surveillance Network (FoodNet). https://www.cdc.gov/foodnet/reports/data/incidence-trends.html. Accessed 04/04/2018 2018.

  • CDC (Centers for Disease Control and Prevention). 2006. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food -- 10 states, United States, 2005. Morbidity and Mortality Weekly Report 55 (14):392–395.

  • Chase, E., and V.J. Harwood. 2011. Comparison of the effects of environmental parameters on growth rates of Vibrio vulnificus biotypes I, II, and III by culture and quantitative PCR analysis. Applied and Environmental Microbiology 77 (12): 4200–4207. https://doi.org/10.1128/aem.00135-11.

    Article  CAS  Google Scholar 

  • Conrads, P.A., E.A. Roehl Jr., R.C. Daamen, and J.B. Cook. 2013. Simulation of salinity intrusion along the Georgia and South Carolina coasts using climate-change scenarios: U.S. Geological Survey.

  • Cooksey, K.E., and B. Wigglesworth-Cooksey. 1995. Adhesion of bacteria and diatoms to surfaces in the sea—a review. Aquatic Microbial Ecology 9 (1): 87–96. https://doi.org/10.3354/ame009087.

    Article  Google Scholar 

  • Deeb, Reem. 2013. Climate change effects on Vibrio bacteria in the Winyah Bay estuary and the projected spread of Vibrio under future climatic scenarios. University of South Carolina, Columbia, SC.

  • Dhillon, G.S., and S. Inamdar. 2014. Storm event patterns of particulate organic carbon (POC) for large storms and differences with dissolved organic carbon (DOC). Biogeochemistry 118 (1–3): 61–81. https://doi.org/10.1007/s10533-013-9905-6.

    Article  CAS  Google Scholar 

  • Emanuel, K. 2017. Assessing the present and future probability of hurricane Harvey’s rainfall. Proceedings of the National Academy of Sciences of the United States of America 114 (48): 12681–12684. https://doi.org/10.1073/pnas.1716222114.

    Article  CAS  Google Scholar 

  • Fries, J.S., G.W. Characklis, and R.T. Noble. 2006. Attachment of fecal indicator bacteria to particles in the Neuse River estuary, NC. Journal of Environmental Engineering-ASCE 132 (10): 1338–1345. https://doi.org/10.1061/(asce)0733-9372(2006)132:10(1338).

    Article  CAS  Google Scholar 

  • Fries, J.S., R.T. Noble, G.M. Kelly, and J.L. Hsieh. 2007. Storm impacts on potential pathogens in estuaries. Eos, Transactions of the American Geophysical Union 88 (8): 93–95.

    Article  Google Scholar 

  • Fries, J.S., G.W. Characklis, and R.T. Noble. 2008. Sediment-water exchange of Vibrio sp and fecal indicator bacteria: Implications for persistence and transport in the Neuse River estuary, North Carolina, USA. Water Research 42 (4–5): 941–950. https://doi.org/10.1016/j.watres.2007.09.006.

    Article  CAS  Google Scholar 

  • Froelich, B., J. Bowen, R. Gonzalez, A. Snedeker, and R. Noble. 2013. Mechanistic and statistical models of total Vibrio abundance in the Neuse River estuary. Water Research 47 (15): 5783–5793. https://doi.org/10.1016/j.watres.2013.06.050.

    Article  CAS  Google Scholar 

  • Griffitt, K.J., and D.J. Grimes. 2013. Abundance and distribution of Vibrio cholerae, V. parahaemolyticus, and V. vulnificus following a major freshwater intrusion into the Mississippi sound. Microbial Ecology 65 (3): 578–583. https://doi.org/10.1007/s00248-013-0203-6.

    Article  Google Scholar 

  • Ho, Hoi, and Burke A. Cunha. 2009. Vibrio infections. Medscape. 12p.

  • Hoi, L., J.L. Larsen, I. Dalsgaard, and A. Dalsgaard. 1998. Occurrence of Vibrio vulnificus biotypes in Danish marine environments. Applied and Environmental Microbiology 64 (1): 7–13.

    CAS  Google Scholar 

  • Jacobs, J. M., M. R. Rhodes, C. W. Brown, R. R. Hood, A. K. Leight, W. Long, and R. Wood. 2010. Predicting the distribution of Vibrio vulnificus in Chesapeake Bay. Oxford, MD: NOAA National Centers for Coastal Ocean Science, Center for Coastal Environmental Health and Biomolecular Research, Cooperative Oxford Laboratory.

  • Johnson, C.N., A.R. Flowers, N.F. Noriea, A.M. Zimmerman, J.C. Bowers, A. DePaola, and D.J. Grimes. 2010. Relationships between environmental factors and pathogenic Vibrios in the northern Gulf of Mexico. Applied and Environmental Microbiology 76 (21): 7076–7084. https://doi.org/10.1128/aem.00697-10.

    Article  CAS  Google Scholar 

  • Jones, M.K., and J.D. Oliver. 2009. Vibrio vulnificus: disease and pathogenesis. Infection and Immunity 77 (5): 1723–1733. https://doi.org/10.1128/iai.01046-08.

    Article  CAS  Google Scholar 

  • Karl, Thomas R., Jerry M. Melillo, and Thomas C. Peterson. 2009. Global climate change impacts in the United States: Cambridge University Press.

  • Kaspar, C.W., and M.L. Tamplin. 1993. Effects of temperature and salinity on the survival of Vibrio-vulnificus in seawater and shellfish. Applied and Environmental Microbiology 59 (8): 2425–2429.

    CAS  Google Scholar 

  • Kaysner, C.A., C. Abeyta, M.M. Wekell, A. Depaola, R.F. Stott, and J.M. Leitch. 1987. Virulent-strains of Vibrio-vulnificus isolated from estuaries of the United-States west coast. Applied and Environmental Microbiology 53 (6): 1349–1351.

    CAS  Google Scholar 

  • Kelly, M.T. 1982. Effect of temperature and salinity on Vibrio (beneckea) vulnificus occurance in a gulf-coast environment. Applied and Environmental Microbiology 44 (4): 820–824.

    CAS  Google Scholar 

  • Lipp, E.K., C. Rodriguez-Palacios, and J.B. Rose. 2001. Occurrence and distribution of the human pathogen Vibrio vulnificus in a subtropical Gulf of Mexico estuary. Hydrobiologia 460 (1/3): 165–173. https://doi.org/10.1023/a:1013127517860.

    Article  CAS  Google Scholar 

  • de Magny, G.C., W. Long, C.W. Brown, R.R. Hood, A. Huq, R. Murtugudde, and R.R. Colwell. 2009. Predicting the distribution of Vibrio spp. in the Chesapeake Bay: a Vibrio cholerae case study. Ecohealth 6 (3): 378–389. https://doi.org/10.1007/s10393-009-0273-6.

    Article  Google Scholar 

  • Martinez-Urtaza, J., C. Baker-Austin, J.L. Jones, A.E. Newton, G.D. Gonzalez-Aviles, and A. DePaola. 2013. Spread of Pacific northwest Vibrio parahaemolyticus strain. New England Journal of Medicine 369 (16): 1573–1574. https://doi.org/10.1056/NEJMc1305535.

    Article  CAS  Google Scholar 

  • Mead, P.S., L. Slutsker, V. Dietz, L.F. McCaig, J.S. Bresee, C. Shapiro, P.M. Griffin, and R.V. Tauxe. 1999. Food-related illness and death in the United States. Emerging Infectious Diseases 5 (5): 607–625.

    Article  CAS  Google Scholar 

  • Motes, M.L., A. DePaola, D.W. Cook, J.E. Veazey, J.C. Hunsucker, W.E. Garthright, R.J. Blodgett, and S.J. Chirtel. 1998. Influence of water temperature and salinity on Vibrio vulnificus in northern gulf and Atlantic Coast oysters (Crassostrea virginica). Applied and Environmental Microbiology 64 (4): 1459–1465.

    CAS  Google Scholar 

  • Oliver, J.D. 2005. Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiology and Infection 133 (3): 383–391. https://doi.org/10.1017/s0950368805003894.

    Article  CAS  Google Scholar 

  • Oliver, J.D. 2015. The biology of Vibrio vulnificus. Microbiology Spectrum 3 (3): 10. https://doi.org/10.1128/microbiolspec.VE-0001-2014.

    Article  Google Scholar 

  • Oliver, J.D., R.A. Warner, and D.R. Cleland. 1983. Distribution of Vibrio-vulnificus and other lactose-fermenting vibrios in the marine-environment. Applied and Environmental Microbiology 45 (3): 985–998.

    CAS  Google Scholar 

  • Oneill, K.R., S.H. Jones, and D.J. Grimes. 1992. Seasonal incidence of Vibrio-vulnificus in the Great Bay estuary of New-Hampshire and Maine. Applied and Environmental Microbiology 58 (10): 3257–3262.

    CAS  Google Scholar 

  • Panicker, G., and A.K. Bej. 2005. Real-time PCR detection of Vibrio vulnificus in oysters: comparison of oligonucleotide primers and probes targeting vvhA. Applied and Environmental Microbiology 71 (10): 5702–5709. https://doi.org/10.1128/aem.71.10.5702-5709.2005.

    Article  CAS  Google Scholar 

  • Pfeffer, C.S., M.F. Hite, and J.D. Oliver. 2003. Ecology of Vibrio vulnificus in estuarine waters of eastern North Carolina. Applied and Environmental Microbiology 69 (6): 3526–3531. https://doi.org/10.1128/aem.69.6.3526-3531.2003.

    Article  CAS  Google Scholar 

  • Randa, M.A., M.F. Polz, and E. Lim. 2004. Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Applied and Environmental Microbiology 70 (9): 5469–5476. https://doi.org/10.1128/aem.70.9.5469-5476.2004.

    Article  CAS  Google Scholar 

  • Scott, Geoffrey I., Dwayne E. Porter, R. Sean Norman, C. Hart Scott, Miguel I. Uyaguari-Diaz, Keith A. Maruya, Steve B. Weisberg et al. 2016. Antibiotics as CECs: an overview of the hazards posed by antibiotics and antibiotic resistance. Frontiers in Marine Science 3 (24). doi:https://doi.org/10.3389/fmars.2016.00024.

  • Shaw, K.S., J.M. Jacobs, and B.C. Crump. 2014. Impact of hurricane Irene on Vibrio vulnificus and Vibrio parahaemolyticus concentrations in surface water, sediment, and cultured oysters in the Chesapeake Bay, MD, USA. Frontiers in Microbiology 5: 10. https://doi.org/10.3389/fmicb.2014.00204.

    Article  Google Scholar 

  • Soto, W., J. Gutierrez, M.D. Remmenga, and M.K. Nishiguchi. 2009. Salinity and temperature effects on physiological responses of Vibrio fischeri from diverse ecological niches. Microbial Ecology 57 (1): 140–150. https://doi.org/10.1007/s00248-008-9412-9.

    Article  CAS  Google Scholar 

  • Thompson, J.R., M.A. Randa, L.A. Marcelino, A. Tomita-Mitchell, E. Lim, and M.F. Polz. 2004. Diversity and dynamics of a North Atlantic coastal Vibrio community. Applied and Environmental Microbiology 70 (7): 4103–4110. https://doi.org/10.1128/aem.70.7.4103-4110.2004.

    Article  CAS  Google Scholar 

  • Trtanj, Juli, Lesley Jantarasami, Joan Brunkard, Tracy Collier, John Jacobs, Erin Lipp, Sandra McLellan et al. 2016. Ch. 6: Climate Impacts on Water-Related Illness. In The Impacts of Climate Change on Human Health in the United States: A Scientific Assessment, 157–188. Washington, DC: U.S. Global Change Research Program.

  • USGCRP. 2014. Southeast and the Caribbean. Climate Change Impacts in the United States: The Third National Climate Assessment: Global Change Research Program.

  • Vezzulli, L., I. Brettar, E. Pezzati, P.C. Reid, R.R. Colwell, M.G. Hofle, and C. Pruzzo. 2012. Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME Journal 6 (1): 21–30. https://doi.org/10.1038/ismej.2011.89.

    Article  Google Scholar 

  • Vezzulli, L., C. Grande, P.C. Reid, P. Helaouet, M. Edwards, M.G. Hofle, I. Brettar, R.R. Colwell, and C. Pruzzo. 2016. Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proceedings of the National Academy of Sciences of the United States of America 113 (34): E5062–E5071. https://doi.org/10.1073/pnas.1609157113.

    Article  CAS  Google Scholar 

  • Wetz, J.J., A.D. Blackwood, J.S. Fries, Z.F. Williams, and R.T. Noble. 2008. Trends in total Vibrio spp. and Vibrio vulnificus concentrations in the eutrophic Neuse River estuary, North Carolina, during storm events. Aquatic Microbial Ecology 53 (1): 141–149. https://doi.org/10.3354/ame01223.

    Article  Google Scholar 

  • Wetz, J.J., A.D. Blackwood, J.S. Fries, Z.F. Williams, and R.T. Noble. 2014. Quantification of Vibrio vulnificus in an estuarine environment: a multi-year analysis using QPCR. Estuaries and Coasts 37 (2): 421–435. https://doi.org/10.1007/s12237-013-9682-4.

    Article  Google Scholar 

  • Williams, T. C., B. A. Froelich, and J. D. Oliver. 2011. Comparison of two selective and differential media for the isolation of Vibrio vulnificus from the environment.

  • Wright, A.C., R.T. Hill, J.A. Johnson, M.C. Roghman, R.R. Colwell, and J.G. Morris. 1996. Distribution of Vibrio vulnificus in the Chesapeake Bay. Applied and Environmental Microbiology 62 (2): 717–724.

    CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by a grant from the National Oceanic and Atmospheric Administration (NOAA) Climate Program Office (grant NA11OAR4310148). The authors wish to acknowledge essential assistance from several staff at the NOAA Center for Coastal Environmental Health and Biomolecular Research, especially Mike Fulton and Marie DeLorenzo who helped direct portions of the microbial research analysis as well as James Daugomah and Blaine West who provided exceptional assistance in the collection of field data. Alison Pierce, a graduate student at the University of South Carolina, also assisted with the laboratory analysis of the Vibrio isolates. Paul Conrads (US Geological Survey) provided assistance with integrating this research with the PRISM2 model. This article is dedicated to the memory of Paul Conrads (d. December 2, 2017), our frequent collaborator and friend.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Tufford.

Additional information

Communicated by Cathleen Wigand

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deeb, R., Tufford, D., Scott, G.I. et al. Impact of Climate Change on Vibrio vulnificus Abundance and Exposure Risk. Estuaries and Coasts 41, 2289–2303 (2018). https://doi.org/10.1007/s12237-018-0424-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-018-0424-5

Keywords

Navigation