Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus

Abstract

Incidence of vibriosis is rising globally, with evidence that changing climatic conditions are influencing environmental factors that enhance growth of pathogenic Vibrio spp. in aquatic ecosystems. To determine the impact of environmental factors on occurrence of pathogenic Vibrio spp., samples were collected in the Chesapeake Bay, Maryland, during 2009 to 2012 and 2019 to 2022. Genetic markers for Vibrio vulnificus (vvhA) and Vibrio parahaemolyticus (tlh, tdh, and trh) were enumerated by direct plating and DNA colony hybridization. Results confirmed seasonality and environmental parameters as predictors. Water temperature showed a linear correlation with vvhA and tlh, and two critical thresholds were observed, an initial increase in detectable numbers (>15°C) and a second increase when maximum counts were recorded (>25°C). Temperature and pathogenic V. parahaemolyticus (tdh and trh) were not strongly correlated; however, the evidence showed that these organisms persist in oyster and sediment at colder temperatures. Salinity (10 to 15 ppt), total chlorophyll a (5 to 25 μg/L), dissolved oxygen (5 to 10 mg/L), and pH (8) were associated with increased abundance of vvhA and tlh. Importantly, a long-term increase in Vibrio spp. numbers was observed in water samples between the two collection periods, specifically at Tangier Sound (lower bay), with the evidence suggesting an extended seasonality for these bacteria in the area. Notably, tlh showed a mean positive increase that was ca. 3-fold overall, with the most significant increase observed during the fall. In conclusion, vibriosis continues to be a risk in the Chesapeake Bay region. A predictive intelligence system to assist decision makers, with respect to climate and human health, is warranted. IMPORTANCE The genus Vibrio includes pathogenic species that are naturally occurring in marine and estuarine environments globally. Routine monitoring for Vibrio species and environmental parameters influencing their incidence is critical to provide a warning system for the public when the risk of infection is high. In this study, occurrence of Vibrio parahaemolyticus and Vibrio vulnificus, both potential human pathogens, in Chesapeake Bay water, oysters, and sediment samples collected over a 13-year period was analyzed. The results provide a confirmation of environmental predictors for these bacteria, notably temperature, salinity, and total chlorophyll a, and their seasonality of occurrence. New findings refine environmental parameter thresholds of culturable Vibrio species and document a long-term increase in Vibrio populations in the Chesapeake Bay. This study provides a valuable foundation for development of predicative risk intelligence models for Vibrio incidence during climate change.

Keywords: Chesapeake Bay; Vibrio parahaemolyticus; Vibrio vulnificus; chlorophyll; climate change; environmental microbiology; pathogens; predictive intelligence; salinity; temperature; virulence determinants.

FIG 1

Map of sampling locations in the Chesapeake Bay. The map shows the eastern seaboard of the United States. The inset shows sampling locations, indicated by red diamonds. The scale bar corresponds to distance using World Map Data from Natural Earth (121).

FIG 2

Box plots of environmental parameters. Boxes summarize distribution by indication of interquartile range (IQR), with the median shown as the center bar of each group. Whiskers represent 1.5 times the IQR. Additional circles indicate outlier values. Shown are environmental parameters for samples collected between 2009 and 2012 (A) and between 2019 and 2022 (B). CR, Chester River; TS, Tangier Sound; CHR, Choptank River; UPR, Upper Patuxent River; WR, Wicomico River.

FIG 3

Box plots of DPCH results. Boxes summarize distribution by indication of IQR, with the median shown as the center bar of each group. Whiskers represent 1.5 times the IQR. Additional circles indicate outlier values. (A and B) DPCH results for samples collected between 2009 and 2012 (A) and between 2009 and 2012 (B). (C to F) Comparison of collection periods at all stations (C), all stations by season (D), Tangier Sound (E), and Tangier Sound by season (F).

FIG 4

Seasonal association of DPCH results. Bar plots show DPCH results on the right axis and temperature values (black lines) on the left. Scatterplots include linear regression, with 95% confidence intervals represented by shaded regions. Correlations among axis variables were respectively generated using Kendall’s tau method. Shown are DPCH results and temperature for samples collected between 2009 and 2012 (A and B) and 2019 to 2022 (C and D).

FIG 5

Association of temperature, salinity, and total chlorophyll a with occurrence of Vibrio vulnificus and Vibrio parahaemolyticus. Three-dimensional scatterplots are shown for temperature, salinity, and total chlorophyll a; marker size and color are indicative of detection and abundance of vvhA (A) and tlh (B). Two-dimensional scatterplots show the association of environmental parameters with direct plating and DNA colony hybridization results and include linear regression, with 95% confidence intervals represented by shaded regions. Correlations among axis variables for temperature and DPCH results were generated using Kendall’s tau method. A nonparametric regression model, i.e., LOESS, was used to visualize the relationship of DPCH results with environmental parameters lacking linear correlation, i.e., salinity and total chlorophyll a. Bar plots represent the percent positive samples above defined hybridization thresholds, following the binning of environmental parameter values. Two-dimensional scatterplots and bar plots are shown for temperature (C and D), salinity (E and F), and total chlorophyll a (G and H).