Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic

Contributed by Rita R. Colwell, June 22, 2016 (sent for review January 20, 2016; reviewed by Craig Baker-Austin, Peter G. Brewer, and Jaime Martinez-Urtaza)
August 8, 2016
113 (34) E5062-E5071

Significance

Long-term ecological and paleontological data analyses indicate climate change is having an impact on marine eukaryotic communities. However, little is known about effects of global warming on marine prokaryotes, which are, by far, the largest living biomass in world oceans. Here, we report, for the first time to our knowledge, that a warming trend in sea surface temperature is strongly associated with spread of vibrios, an important group of marine prokaryotes, and emergence of human diseases caused by these pathogens. Our results are based on formalin-preserved plankton samples collected in the past half-century from the temperate North Atlantic.

Abstract

Climate change is having a dramatic impact on marine animal and plant communities but little is known of its influence on marine prokaryotes, which represent the largest living biomass in the world oceans and play a fundamental role in maintaining life on our planet. In this study, for the first time to our knowledge, experimental evidence is provided on the link between multidecadal climatic variability in the temperate North Atlantic and the presence and spread of an important group of marine prokaryotes, the vibrios, which are responsible for several infections in both humans and animals. Using archived formalin-preserved plankton samples collected by the Continuous Plankton Recorder survey over the past half-century (1958–2011), we assessed retrospectively the relative abundance of vibrios, including human pathogens, in nine areas of the North Atlantic and North Sea and showed correlation with climate and plankton changes. Generalized additive models revealed that long-term increase in Vibrio abundance is promoted by increasing sea surface temperatures (up to ∼1.5 °C over the past 54 y) and is positively correlated with the Northern Hemisphere Temperature (NHT) and Atlantic Multidecadal Oscillation (AMO) climatic indices (P < 0.001). Such increases are associated with an unprecedented occurrence of environmentally acquired Vibrio infections in the human population of Northern Europe and the Atlantic coast of the United States in recent years.

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Acknowledgments

We thank all past and present members and supporters of the CPR survey whose efforts have enabled the establishment and long-term maintenance of the CPR dataset and the archived samples used in this study. We are particularly indebted to Robert Camp (Sir Alister Hardy Foundation for Ocean Science) for helpful assistance and advice in the selection and analysis of CPR samples. We also greatly thank and acknowledge Dr. Paolo Vassallo (DISTAV, University of Genoa) for his valuable help with GAM analysis. This work was supported by the Royal Society “International Exchanges 2013/R2(inc CNRS)” (Grant IE130623) and the FP7-AQUAVALENS project (Grant 311846). The CPR survey is supported by the UK Natural Environment Research Council and the UK Department for Environment, Food, and Rural Affairs. The Johns Hopkins University and the University of Maryland, College Park (NIH Grant 2RO1A1039129-11A2) are also acknowledged.

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References

1
J Hansen, R Ruedy, M Sato, K Lo, Global surface temperature change. Rev Geophys 48, RG4004 (2010).
2
PC Reid, G Gorick, M Edwards Climate Change and European Marine Ecosystem Research (Sir Alister Hardy Foundation for Ocean Science, Plymouth, UK, 2011).
3
; IPCC Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Inter-Governmental Panel on Climate Change, eds TF Stocker, et al. (Cambridge Univ Press, Cambridge, UK, 2013).
4
ES Poloczanska, et al., Global imprint of climate change on marine life. Nat Clim Chang 3, 919–925 (2013).
5
WB Whitman, DC Coleman, WJ Wiebe, Prokaryotes: The unseen majority. Proc Natl Acad Sci USA 95, 6578–6583 (1998).
6
CD Harvell, et al., Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162 (2002).
7
JJ Farmer, JM Janda, FW Brenner, DN Cameron, KM Birkhead, Genus I. Vibrio Pacini 1854. Bergey’s Manual of Systematic Bacteriology, eds DJ Brenner, NR Krieg, JR Staley (Springer Science Business Media, Inc., 2nd Ed, New York) Vol 2, 494–546 (2005).
8
RR Colwell, Global climate and infectious disease: The cholera paradigm. Science 274, 2025–2031 (1996).
9
; WHO, Cholera: Fact Sheet No. 107. Available at www.who.int/mediacentre/factsheets/fs107/en/. Accessed July 18, 2016. (2015).
10
GB Nair, et al., Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin Microbiol Rev 20, 39–48 (2007).
11
EJ Nelson, JB Harris, Jr JG Morris, SB Calderwood, A Camilli, Cholera transmission: The host, pathogen and bacteriophage dynamic. Nat Rev Microbiol 7, 693–702 (2009).
12
M Pascual, X Rodó, SP Ellner, R Colwell, MJ Bouma, Cholera dynamics and El Niño-Southern oscillation. Science 289, 1766–1769 (2000).
13
J Martinez-Urtaza, JC Bowers, J Trinanes, A DePaola, Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses. Food Res Int 43, 1780–1790 (2010).
14
JC Semenza, et al., Climate change impact assessment of food- and waterborne diseases. Crit Rev Environ Sci Technol 42, 857–890 (2012).
15
C Frank, M Littman, K Alpers, J Hallauer, Vibrio vulnificus wound infections after contact with the Baltic Sea, Germany. Euro Surveill 11, E060817.1 (2006).
16
Y Andersson, K Ekdahl, Wound infections due to Vibrio cholerae in Sweden after swimming in the Baltic Sea, summer 2006. Euro Surveill 11, E060803.2 (2006).
17
FM Schets, et al., Vibrio alginolyticus infections in the Netherlands after swimming in the North Sea. Euro Surveill 11, E061109.3 (2006).
18
C Baker-Austin, et al., Emerging Vibrio risk at high latitudes in response to ocean warming. Nat Clim Chang 3, 73–77 (2013).
19
L Vezzulli, et al., Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. Environ Microbiol; VibrioSea Consortium 12, 2007–2019 (2010).
20
L Vezzulli, C Pruzzo, A Huq, RR Colwell, Environmental reservoirs of Vibrio cholerae and their role in cholera. Environ Microbiol Rep 2, 27–33 (2010).
21
L Vezzulli, et al., Long-term effects of ocean warming on the prokaryotic community: Evidence from the vibrios. ISME J 6, 21–30 (2012).
22
L Vezzulli, RR Colwell, C Pruzzo, Ocean warming and spread of pathogenic vibrios in the aquatic environment. Microb Ecol 65, 817–825 (2013).
23
H Hátún, et al., Large bio-geographical shifts in the north-eastern Atlantic Ocean: From the subpolar gyre, via plankton, to blue whiting and pilot whales. Prog Oceanogr 80, 149–162 (2009).
24
S Alvarez-Fernandez, H Lindeboom, E Meesters, Temporal changes in plankton of the North Sea: Community shifts and environmental drivers. Mar Ecol Prog Ser 462, 21–38 (2012).
25
G Beaugrand, X Harlay, M Edwards, Detecting plankton shifts in the North Sea: A new abrupt eco-system shift between 1996 and 2003. Mar Ecol Prog Ser 502, 85–104 (2014).
26
V Harris, M Edwards, SC Olhede, Multidecadal Atlantic climate variability and its impact on marine pelagic communities. J Mar Syst 133, 55–69 (2014).
27
ME Schlesinger, N Ramankutty, An oscillation in the global climate system of period 65–70 years. Nature 367, 723–726 (1994).
28
DB Enfield, AM Mestas-Nunez, PJ Trimble, The Atlantic Multidecadal Oscillation and its relation to rainfall and river flows in the continental U.S. Geophys Res Lett 28, 2077–2080 (2001).
29
PD Jones, T Jonsson, D Wheeler, Extension to the North Atlantic Oscillation using early instrumental pressure observations from Gibraltar and South-West Iceland. Int J Climatol 17, 1433–1450 (1997).
30
JM Wallace, North Atlantic Oscillation/annular mode: Two paradigms–one phenomenon. Q J R Meteorol Soc 126, 791–805 (2000).
31
JM Wallace, DS Gutzler, Teleconnections in the geopotential height field during the Northern Hemisphere winter. Monthly Weather Review 109, 784–812 (1980).
32
JW Hurrell, Decadal trends in the North Atlantic Oscillation: Regional temperatures and precipitation. Science 269, 676–679 (1995).
33
DWJ Thompson, JM Wallace, JJ Kennedy, PD Jones, An abrupt drop in Northern Hemisphere sea surface temperature around 1970. Nature 467, 444–447 (2010).
34
T Delworth, ME Mann, Observed and simulated multidecadal variability in the Northern Hemisphere. Clim Dyn 16, 661–676 (2000).
35
JW Hurrell, et al., The North Atlantic Oscillation: Climate Significance and Environmental Impact, Geophysical Monograph Series 134, eds Hurrell JW, Kushnir Y, Ottersen G, Visbeck M (American Geophysical Union, Washington, DC). (2003).
36
RR Dickson, WR Turrell, The NAO: The dominant atmospheric process affecting oceanic variability in home, middle and distant waters of European salmon. The Ocean Life of Atlantic Salmon-Environmental and Biological Factors Influencing Survival, ed D Mills (Fishing News Books, Oxford, UK), pp. 92–115 (2000).
37
AG Barnston, RE Livezey, Classification, seasonality and persistence of low-frequency atmospheric circulation patterns. Monthly Weather Review 115, 1083–1126 (1987).
38
AH Taylor, JA Stephens, Latitudinal displacements of the Gulf Stream and their relation to changes in temperature and zooplankton abundance in the NE Atlantic. Oceanologica Acta 3, 145–149 (1980).
39
JD Oliver, C Pruzzo, L Vezzulli, JB Kaper, Vibrio species. Food Microbiology: Fundamentals and Frontiers, eds MP Doyle, RL Buchanan (ASM Press, 4th Ed, Washington, DC, 2013).
40
C Pruzzo, L Vezzulli, RR Colwell, Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10, 1400–1410 (2008).
41
Seeligmann CT, et al. (2008) Phytoplankton-linked viable non-culturable Vibrio cholerae O1 (VNC) from rivers in Tucuman, Argentina. J Plankton Res 30(4):367–377.
42
KR Frischkorn, A Stojanovski, R Paranjpye, Vibrio parahaemolyticus type IV pili mediate interactions with diatom-derived chitin and point to an unexplored mechanism of environmental persistence. Environ Microbiol 15, 1416–1427 (2013).
43
L Vezzulli, M Fabiano, Sediment biochemical and microbial variables for the evaluation of trophic status along the Italian and Albanian Continental Shelves. J Mar Biol Assoc U.K. 86, 27–37 (2006).
44
EK Lipp, A Huq, RR Colwell, Effects of global climate on infectious disease: The cholera model. Clin Microbiol Rev 15, 757–770 (2002).
45
JW Turner, B Good, D Cole, EK Lipp, Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J 3, 1082–1092 (2009).
46
A McQuatters-Gollop, et al., Is there a decline in marine phytoplankton? Nature 472, E6–E7, discussion E8–E9 (2011).
47
SL Hinder, et al., Changes in marine dinoflagellate and diatom abundance under climate change. Nat Clim Chang 2, 271–275 (2012).
48
CR Main, LR Salvitti, EB Whereat, KJ Coyne, Community-level and species-specific associations between phytoplankton and particle-associated Vibrio species in Delaware’s inland bays. Appl Environ Microbiol 81, 5703–5713 (2015).
49
M Stauder, L Vezzulli, E Pezzati, B Repetto, C Pruzzo, Temperature affects Vibrio cholerae O1 El Tor persistence in the aquatic environment via an enhanced expression of GbpA and MSHA adhesins. Environ Microbiol Rep 2, 140–144 (2010).
50
G Beaugrand, PC Reid, F Ibañez, JA Lindley, M Edwards, Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296, 1692–1694 (2002).
51
P Helaouët, G Beaugrand, PC Reid, Macrophysiology of Calanus finmarchicus in the North Atlantic Ocean. Prog Oceanogr 91, 217–228 (2011).
52
HO Pörtner, Oxygen- and capacity-limitation of thermal tolerance: A matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213, 881–893 (2010).
53
AF Hofmann, ET Peltzer, PG Brewer, Kinetic bottlenecks to chemical exchange rates for deep-sea animals—Part 1: Oxygen. Biogeosciences 9, 13817–13856 (2013).
54
J Garzke, SM Ismar, U Sommer, Climate change affects low trophic level marine consumers: Warming decreases copepod size and abundance. Oecologia 177, 849–860 (2015).
55
TK Rawlings, GM Ruiz, RR Colwell, Association of Vibrio cholerae O1 El Tor and O139 Bengal with the Copepods Acartia tonsa and Eurytemora affinis. Appl Environ Microbiol 73, 7926–7933 (2007).
56
A Huq, et al., Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl Environ Microbiol 45, 275–283 (1983).
57
N Binsztein, et al., Viable but nonculturable Vibrio cholerae O1 in the aquatic environment of Argentina. Appl Environ Microbiol 70, 7481–7486 (2004).
58
ML Lizárraga-Partida, et al., Association of Vibrio cholerae with plankton in coastal areas of Mexico. Environ Microbiol 11, 201–208 (2009).
59
GC de Magny, et al., Role of zooplankton diversity in Vibrio cholerae population dynamics and in the incidence of cholera in the Bangladesh Sundarbans. Appl Environ Microbiol 77, 6125–6132 (2011).
60
A Newton, M Kendall, DJ Vugia, OL Henao, BE Mahon, Increasing rates of vibriosis in the United States, 1996-2010: Review of surveillance data from 2 systems. Clin Infect Dis 54, S391–S395 (2012).
61
J Martinez-Urtaza, et al., Pandemic Vibrio parahaemolyticus O3:K6, Europe. Emerg Infect Dis 11, 1319–1320 (2005).
62
FP Lima, DS Wethey, Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3, 704 (2012).
63
KC Rice, JD Jastram, Rising air and stream-water temperatures in Chesapeake Bay region, USA. Clim Change 128, 127–138 (2015).
64
LE Escobar, et al., A global map of suitability for coastal Vibrio cholerae under current and future climate conditions. Acta Trop 149, 202–211 (2015).
65
PC Reid, JM Colebrook, JBL Matthews, J Aiken, The Continuous Plankton Recorder: Concepts and history, from Plankton Indicator to undulating recorders. Prog Oceanogr 58, 117–173 (2003).
66
SD Batten, et al., CPR sampling: The technical background, materials and methods, consistency and comparability. Prog Oceanogr 58, 193–215 (2003).
67
AJ Warner, GC Hays, Sampling by the Continuous Plankton Recorder survey. Prog Oceanogr 34, 237–256 (1994).
68
L Vezzulli, PC Reid, The CPR survey (1948–1997): A gridded database browser of plankton abundance in the North Sea. Prog Oceanogr 58, 327–336 (2003).
69
JR Thompson, et al., Diversity and dynamics of a north atlantic coastal Vibrio community. Appl Environ Microbiol 70, 4103–4110 (2004).
70
ML Sogin, et al., Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103, 12115–12120 (2006).
71
SG Acinas, LA Marcelino, V Klepac-Ceraj, MF Polz, Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186, 2629–2635 (2004).
72
KA Kormas, Interpreting diversity of Proteobacteria based on 16S rRNA gene copy number. Proteobacteria: Phylogeny, Metabolic Diversity and Ecological Effects, ed ML Sezenna (Nova Publishers, Hauppauge, NY), pp. 73–89 (2011).
73
L Vezzulli, et al., gbpA as a novel qPCR target for the species-specific detection of Vibrio cholerae O1, O139, non-O1/non-O139 in Environmental, Stool, and Historical Continuous Plankton Recorder Samples. PLoS One 10, e0123983 (2015).
74
MS Campbell, AC Wright, Real-time PCR analysis of Vibrio vulnificus from oysters. Appl Environ Microbiol 69, 7137–7144 (2003).
75
JL Nordstrom, MC Vickery, GM Blackstone, SL Murray, A DePaola, Development of a multiplex real-time PCR assay with an internal amplification control for the detection of total and pathogenic Vibrio parahaemolyticus bacteria in oysters. Appl Environ Microbiol 73, 5840–5847 (2007).
76
AJ Richardson, et al., Using continuous plankton recorder data. Prog Oceanogr 68, 27–74 (2006).
77
P Legendre, L Legendre, Numerical ecology. Developments in Environmental Modelling (Elsevier Science BV, 3rd Ed, Amsterdam) Vol 24 (2012).
78
D Borcard, P Legendre, All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Modell 153, 51–68 (2002).
79
S Dray, P Legendre, P Peres-Neto, Spatial modelling: A comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Modell 196, 483–493 (2006).
80
DG Johns, PC Reid An Overview of Plankton Ecology in the North Sea. Technical Report TR_005 for Strategic Environmental Assessment–SEA2 (Sir Alister Hardy Foundation for Ocean Science, Plymouth, UK, 2001).
81
T Hastie, R Tibshirani, Exploring the nature of covariate effects in the proportional hazards model. Biometrics 46, 1005–1016 (1990).
82
SN Wood Generalized Additive Models: An Introduction with R. Texts in Statistical Science (Chapman and Hall/CRC Press, Boca Raton, FL, 2006).
83
J Martinez-Urtaza, et al., Ecological determinants of the occurrence and dynamics of Vibrio parahaemolyticus in offshore areas. ISME J 6, 994–1006 (2012).
84
D Ruppert, MP Wand, RJ Carroll Semiparametric Regression (Cambridge Univ Press, Cambridge, UK, 2003).
85
L Vezzulli, PS Dowland, PC Reid, EK Hylton, Gridded Database Browser of North Sea Plankton, Version 1.1: Fifty-Four Years (1948–2001) of Monthly Plankton Abundance from the Continuous Plankton Recorder (CPR) Survey (Sir Alister Hardy Foundation, Plymouth, UK). Available at cpr.cscan.org/. Accessed July 18, 2016. (2007).
86
IK Crain, BK Bhattacharyya, Treatment of non-equispaced two-dimensional data with a digital computer. Geoexploration 5, 173–194 (1967).
87
JM Colebrook, The Continuous Plankton Recorder survey: Automatic data processing methods. Bull Mar Ecol 8, 123–142 (1975).
88
WL Hooper, GI Barrow, DJN McNab, Vibrio parahaemolyticus food-poisoning in Britain. Lancet 1, 1100–1102 (1974).
89
A Mertens, J Nagler, W Hansen, E Gepts-Friedenreich, Halophilic, lactose-positive Vibrio in a case of fatal septicemia. J Clin Microbiol 9, 233–235 (1979).
90
HK Andersen, Vibrio vulnificus. Ugeskr Laeger 153, 2361–2362. Danish (1991).
91
J Veenstra, et al., Extra-intestinale infecties door Vibrio spp. in Nederland [Extra-intestinal infections caused by Vibrio spp. in The Netherlands]. Ned Tijdschr Geneeskd 137, 654–657. Dutch (1993).
92
GD Reilly, CA Reilly, EG Smith, C Baker-Austin, Vibrio alginolyticus-associated wound infection acquired in British waters, Guernsey, July 2011. Euro Surveill 16, 19994 (2011).

Information & Authors

Information

Published in

The cover image for PNAS Vol.113; No.34
Proceedings of the National Academy of Sciences
Vol. 113 | No. 34
August 23, 2016
PubMed: 27503882

Classifications

Submission history

Published online: August 8, 2016
Published in issue: August 23, 2016

Keywords

  1. climate
  2. Vibrio
  3. prokaryotes
  4. infections
  5. North Atlantic

Acknowledgments

We thank all past and present members and supporters of the CPR survey whose efforts have enabled the establishment and long-term maintenance of the CPR dataset and the archived samples used in this study. We are particularly indebted to Robert Camp (Sir Alister Hardy Foundation for Ocean Science) for helpful assistance and advice in the selection and analysis of CPR samples. We also greatly thank and acknowledge Dr. Paolo Vassallo (DISTAV, University of Genoa) for his valuable help with GAM analysis. This work was supported by the Royal Society “International Exchanges 2013/R2(inc CNRS)” (Grant IE130623) and the FP7-AQUAVALENS project (Grant 311846). The CPR survey is supported by the UK Natural Environment Research Council and the UK Department for Environment, Food, and Rural Affairs. The Johns Hopkins University and the University of Maryland, College Park (NIH Grant 2RO1A1039129-11A2) are also acknowledged.

Authors

Affiliations

Luigi Vezzulli1 [email protected]
Department of Earth, Environmental, and Life Sciences, University of Genoa, 16132 Genoa, Italy;
Chiara Grande
Department of Earth, Environmental, and Life Sciences, University of Genoa, 16132 Genoa, Italy;
Philip C. Reid
Sir Alister Hardy Foundation for Ocean Science, Plymouth PL1 2PB, United Kingdom;
Pierre Hélaouët
Sir Alister Hardy Foundation for Ocean Science, Plymouth PL1 2PB, United Kingdom;
Martin Edwards
Sir Alister Hardy Foundation for Ocean Science, Plymouth PL1 2PB, United Kingdom;
Institute of Marine Studies, University of Plymouth, Plymouth PL4 8AA, United Kingdom;
Manfred G. Höfle
Department of Vaccinology and Applied Microbiology, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany;
Ingrid Brettar
Department of Vaccinology and Applied Microbiology, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany;
Rita R. Colwell1 [email protected]
Maryland Pathogen Research Institute and Center of Bioinformatics and Computational Biology, University of Maryland, College Park, MD 20742;
Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205
Carla Pruzzo
Department of Earth, Environmental, and Life Sciences, University of Genoa, 16132 Genoa, Italy;

Notes

1
To whom correspondence may be addressed. Email: [email protected] or [email protected].
Author contributions: L.V., R.R.C., and C.P. designed research; L.V. and C.G. performed research; L.V., C.G., M.G.H., and I.B. contributed new reagents/analytic tools; L.V., C.G., P.C.R., P.H., M.E., M.G.H., I.B., R.R.C., and C.P. analyzed data; and L.V., R.R.C., and C.P. wrote the paper.
Reviewers: C.B.-A., Centre for Environment Fisheries and Aquaculture Science; P.G.B., Monterey Bay Aquarium Research Institute; and J.M.-U., University of Bath.

Competing Interests

The authors declare no conflict of interest.

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    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
    • Vol. 113
    • No. 34
    • pp. 9381-E5091

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