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

Keywords: North Atlantic; Vibrio; climate; infections; prokaryotes.

Fig. 1.

Sampling areas in the temperate North Atlantic where CPR samples were collected for retrospective molecular studies of Vibrio populations over the period 1958–2011 [each area is scaled to an actual size of 1° longitude × 1° latitude (i.e., ∼32 × 60 nautical miles)].

Fig. 2.

Change in North Atlantic SST (degrees Celsius) over the study period calculated as delta between SST averaged over the years 2000–2011 and 1890–1958. Hot colors indicate areas of warming. Sampling areas are indicated as black dots on the map.

Fig. 3.

Multidecadal relationship between Vibrio prokaryote abundance and SST in the temperate North Atlantic and North Sea. Standardized (Z) VAI data (blue triangles) are superimposed to standardized (Z) SST monthly means time series data (red line) for nine geographic areas in the temperate North Atlantic. The presence of the human pathogenic species V. cholerae (V.c., yellow bacterial cell), V. parahaemolyticus (V.p., green bacterial cell), and V. vulnificus (V.v., pink bacterial cell) is shown. Z-values were obtained by subtracting the population mean and dividing the difference by the SD. **P < 0.05, Pearson correlation analysis.

Fig. 4.

Effects of climate variables in the GAM explaining Vibrio abundance (Vibrio index) in the North Atlantic region. Solid lines represent the estimated smooth function, and dashed lines represent the 95% confidence bounds. The y-axis captions are the effective degrees of freedom for each term. (A) Northern Hemisphere mean land–ocean temperature (NHT) index (deviance explained = 11.3%; **P < 0.001). (B) SST (deviance explained = 15.7%; **P < 0.001). (C) AMO index (deviance explained = 19.5%; **P < 0.001). (D) EAP (deviance explained = 19.4%; P > 0.05). (E) NAO index (deviance explained = 13.2%; P > 0.05). (F) GSNW index (deviance explained = 17.4%; P > 0.05).

Fig. S1.

Maps of average long-term SST (A) and salinity values (B) for the North Atlantic Ocean (1958–2011). Data were downloaded from the Sir Alister Hardy Foundation for Ocean Science and Centre for Security, Communications, and Network Research, Plymouth University, average long-term temperature for the North Atlantic (cpr.cscan.org/pages/WebCPR/NAWebCPRWizard8.asp?data=climatology&variable=TEMP&output=chart&plot=Plot). Sampling areas are indicated as black dots on the map. PSU, practical salinity unit.

Fig. 5.

Multidecadal relationship between Vibrio prokaryote abundance, plankton abundance, and plankton community structure in the North Sea for 1958–2011. (A) Standardized (Z) Vibrio index (VAI) data (blue triangles) are superimposed to broad-scale submodel monthly time series for the PCI (green line) and TotCop (brown line) data for the northern and southern North Sea. The presence of human pathogenic species V. cholerae (V.c., yellow bacterial cell), V. parahaemolyticus (V.p., green bacterial cell), and V. vulnificus (V.v., pink bacterial cell) is shown. Pearson correlation analysis was performed between the VAI and corresponding plankton submodel data for the month of August 1958–2011. (B) Month-by-year contour plots of plankton abundance for the 10 most abundant phytoplankton and zooplankton species in the northern and southern North Sea, according to Johns and Reid (80). The phytoplankton species are as follows: Ceratium furca (C.furca), Ceratium fusus (C.fusus), Ceratium horridum (C.horr), Ceratium lineatum (C.lin), Ceratium longipes (C.long), Ceratium macroceros (C.macro), Ceratium tripos (C.tripos), Chaetoceros(Hyalochaete) spp. (Hyal), Chaetoceros(Phaeoceros) spp. (Phaeo), Rhizosolenia imbricata (R.Imb), and Thalassiosira spp. (Thalass). The zooplankton species are as follows: Acartia spp. (Acartia), Calanus finmarchicus (Cal.fin), Calanus helgolandicus (Cal.hel), Calanus I–IV (CalI-IV), Calanus traverse (CalTrav), Echinoderm larvae (Ech.larv), Evadne spp. (Evadne), Oithona spp. (Oithona), Para-Pseudocalanus spp. (PPcal), Podon spp. (Podon), Pseudocalanus adult (Pcal.ad), and Temora longicornis (Temora l).

Fig. 6.

Cases of Vibrio infections reported for Northern European countries (including the Baltic Sea) and Atlantic coast of the United States, 1958–2011. The presence of potential human pathogenic species in CPR samples collected in the same macroareas is also shown. The presence of human pathogenic species V. cholerae (V.c., yellow bacterial cell), V. parahaemolyticus (V.p., green bacterial cell), and V. vulnificus (V.v., pink bacterial cell) is shown.

Fig. S2.

Scalogram of the PCI and TotCop structure along the temporal transect (time series) in both the southern and northern North Sea. The abscissa represents the 199 distance-based MEM eigenfunctions with positive Moran’s I. The size of the circles represents the proportion of variance (as a percentage of R² of the total model) explained by each eigenfunction. The eigenfunctions selected by forward selection (P ≤ 0.05) are identified by red circles (34 for PCI, 58 for TotCop).