Genomic diversity of Vibrio spp. and metagenomic analysis of pathogens in Florida Gulf coastal waters following Hurricane Ian.

Changing climatic conditions influence parameters associated with the growth of pathogenic Vibrio spp. in the environment and, hence, are linked to increased incidence of vibriosis. Between 1992 and 2022, a long-term increase in Vibrio spp. infections was reported in Florida, USA. Furthermore, a spike in Vibrio spp. infections was reported post Hurricane Ian, a category five storm that made landfall in Florida on 28 September 2022. During October 2022, water and oyster samples were collected from three stations in Lee County in an area significantly impacted by Ian. Vibrio spp. were isolated, and whole-genome sequencing and phylogenetic analysis were done, with a focus on Vibrio parahaemolyticus and Vibrio vulnificus to provide genetic insight into pathogenic strains circulating in the environment. Metagenomic analysis of water samples provided insight with respect to human health-related factors, notably the detection of approximately 12 pathogenic Vibrio spp., virulence and antibiotic resistance genes, and mobile genetic elements, including the SXT/R391 family of integrative conjugative elements. Environmental parameters were monitored as part of a long-term time series analysis done using satellite remote sensing. In addition to anomalous rainfall and storm surge, changes in sea surface temperature and chlorophyll concentration during and after Ian favored the growth of Vibrio spp. In conclusion, genetic analysis coupled with environmental data and remote sensing provides useful public health information and, hence, constitute a valuable tool to proactively detect and characterize environmental pathogens, notably vibrios. These data can aid the development of early warning systems by yielding a larger source of information for public health during climate change. Evidence suggests warming temperatures are associated with the spread of potentially pathogenic Vibrio spp. and the emergence of human disease globally. Following Hurricane Ian, the State of Florida reported a sharp increase in the number of reported Vibrio spp. infections and deaths. Hence, monitoring of pathogens, including vibrios, and environmental parameters influencing their occurrence is critical to public health. Here, DNA sequencing was used to investigate the genomic diversity of Vibrio parahaemolyticus and Vibrio vulnificus, both potential human pathogens, in Florida coastal waters post Hurricane Ian, in October 2022. Additionally, the microbial community of water samples was profiled to detect the presence of Vibrio spp. and other microorganisms (bacteria, fungi, protists, and viruses) present in the samples. Long-term environmental data analysis showed changes in environmental parameters during and after Ian were optimal for the growth of Vibrio spp. and related pathogens. Collectively, results will be used to develop predictive risk models during climate change.

Environmental Factors Associated with Incidence and Distribution of V. parahaemolyticus and V. vulnificus in Chesapeake Bay, Maryland, USA: A three-year case study.

Members of the genus Vibrio are ecologically significant bacteria native to aquatic ecosystems globally, and a few can cause diseases in humans. Vibrio-related illnesses have increased in recent years, primarily attributed to changing environmental conditions. Therefore, understanding the role of environmental factors in the occurrence and growth of pathogenic strains is crucial for public health. Water, oyster, and sediment samples were collected between 2009 and 2012 from Chester River and Tangier Sound sites in Chesapeake Bay, Maryland, USA, to investigate the relationship between water temperature, salinity, and chlorophyll with the incidence and distribution of Vibrio parahaemolyticus (VP) and Vibrio vulnificus (VV). Odds ratio analysis was used to determine association between the likelihood of VP and VV presence and these environmental variables. Results suggested that water temperature threshold of 20°C or higher was associated with an increased risk, favoring the incidence of Vibrio spp. A significant difference in salinity was observed between the two sampling sites, with distinct ranges showing high odds ratio for Vibrio incidence, especially in water and sediment, emphasizing the impact of salinity on VP and VV incidence and distribution. Notably, salinity between 9-20 PPT consistently favored the Vibrio incidence across all samples. Relationship between chlorophyll concentrations and VP and VV incidence varied depending on sample type. However, chlorophyll range of 0-10 µg/L was identified as critical in oyster samples for both vibrios. Analysis of odds ratios for water samples demonstrated consistent outcomes across all environmental parameters, indicating water samples offer a more reliable indicator of Vibrio spp. incidence.

Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus.

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.

Environmental parameters associated with incidence and transmission of pathogenic Vibrio spp.

Vibrio spp. thrive in warm water and moderate salinity, and they are associated with aquatic invertebrates, notably crustaceans and zooplankton. At least 12 Vibrio spp. are known to cause infection in humans, and Vibrio cholerae is well documented as the etiological agent of pandemic cholera. Pathogenic non-cholera Vibrio spp., e.g., Vibrio parahaemolyticus and Vibrio vulnificus, cause gastroenteritis, septicemia, and other extra-intestinal infections. Incidence of vibriosis is rising globally, with evidence that anthropogenic factors, primarily emissions of carbon dioxide associated with atmospheric warming and more frequent and intense heatwaves, significantly influence environmental parameters, e.g., temperature, salinity, and nutrients, all of which can enhance growth of Vibrio spp. in aquatic ecosystems. It is not possible to eliminate Vibrio spp., as they are autochthonous to the aquatic environment and many play a critical role in carbon and nitrogen cycling. Risk prediction models provide an early warning that is essential for safeguarding public health. This is especially important for regions of the world vulnerable to infrastructure instability, including lack of 'water, sanitation, and hygiene' (WASH), and a less resilient infrastructure that is vulnerable to natural calamity, e.g., hurricanes, floods, and earthquakes, and/or social disruption and civil unrest, arising from war, coups, political crisis, and economic recession. Incorporating environmental, social, and behavioural parameters into such models allows improved prediction, particularly of cholera epidemics. We have reported that damage to WASH infrastructure, coupled with elevated air temperatures and followed by above average rainfall, promotes exposure of a population to contaminated water and increases the risk of an outbreak of cholera. Interestingly, global predictive risk models successful for cholera have the potential, with modification, to predict diseases caused by other clinically relevant Vibrio spp. In the research reported here, the focus was on environmental parameters associated with incidence and distribution of clinically relevant Vibrio spp. and their role in disease transmission. In addition, molecular methods designed for detection and enumeration proved useful for predictive modelling and are described, namely in the context of prediction of environmental conditions favourable to Vibrio spp., hence human health risk.

Population vulnerability to biannual cholera outbreaks and associated macro-scale drivers in the Bengal Delta.

The highly populated floodplains of the Bengal Delta have a long history of endemic and epidemic cholera outbreaks, both coastal and inland. Previous studies have not addressed the spatio-temporal dynamics of population vulnerability related to the influence of underlying large-scale processes. We analyzed spatial and temporal variability of cholera incidence across six surveillance sites in the Bengal Delta and their association with regional hydroclimatic and environmental drivers. More specifically, we use salinity and flood inundation modeling across the vulnerable districts of Bangladesh to test earlier proposed hypotheses on the role of these environmental variables. Our results show strong influence of seasonal and interannual variability in estuarine salinity on spring outbreaks and inland flooding on fall outbreaks. A large segment of the population in the Bengal Delta floodplains remain vulnerable to these biannual cholera transmission mechanisms that provide ecologic and environmental conditions for outbreaks over large geographic regions.

Satellite Remote Sensing of Space-Time Plankton Variability in the Bay of Bengal: Connections to Cholera Outbreaks.

Cholera bacteria exhibit strong association with coastal plankton. Characterization of space-time variability of chlorophyll, a surrogate for plankton abundance, in Northern Bay of Bengal is an essential first step to develop any methodology for predicting cholera outbreaks in the Bengal Delta region using remote sensing. This study quantifies the space-time distribution of chlorophyll, using data from SeaWiFS, in the Bay of Bengal region using ten years of satellite data. Variability of chlorophyll at daily scale, irrespective of spatial averaging, resembles white noise. At a monthly scale, chlorophyll shows distinct seasonality and chlorophyll values are significantly higher close to the coast than in the offshore regions. At pixel level (9 km) on monthly scale, on the other hand, chlorophyll does not exhibit much persistence in time. With increased spatial averaging, temporal persistence of chlorophyll increases and lag one autocorrelation stabilizes around 0.60 for 1296 km(2) or larger areal averages. In contrast to the offshore regions, spatial analyses of chlorophyll suggest that only coastal region has a stable correlation length of 100 km. Presence (absence) of correlation length in the coastal (offshore) regions, indicate that the two regions may have two separate processes controlling the production a phytoplankton This study puts a lower limit on space-time averaging of satellite measured plankton at 1296 km(2)-monthly scale to establish relationships with cholera incidence in Bengal Delta.

Warming oceans, phytoplankton, and river discharge: implications for cholera outbreaks.

Phytoplankton abundance is inversely related to sea surface temperature (SST). However, a positive relationship is observed between SST and phytoplankton abundance in coastal waters of Bay of Bengal. This has led to an assertion that in a warming climate, rise in SST may increase phytoplankton blooms and, therefore, cholera outbreaks. Here, we explain why a positive SST-phytoplankton relationship exists in the Bay of Bengal and the implications of such a relationship on cholera dynamics. We found clear evidence of two independent physical drivers for phytoplankton abundance. The first one is the widely accepted phytoplankton blooming produced by the upwelling of cold, nutrient-rich deep ocean waters. The second, which explains the Bay of Bengal findings, is coastal phytoplankton blooming during high river discharges with terrestrial nutrients. Causal mechanisms should be understood when associating SST with phytoplankton and subsequent cholera outbreaks in regions where freshwater discharge are a predominant mechanism for phytoplankton production.

Tracking Cholera in Coastal Regions using Satellite Observations.

Cholera remains a significant health threat across the globe. The pattern and magnitude of the seven global pandemics suggest that cholera outbreaks primarily originate in coastal regions and then spread inland through secondary means. Cholera bacteria show strong association with plankton abundance in coastal ecosystems. This review study investigates relationship(s) between cholera incidence and coastal processes and explores utility of using remote sensing data to track coastal plankton blooms, using chlorophyll as a surrogate variable for plankton abundance, and subsequent cholera outbreaks. Most studies over the last several decades have primarily focused on the microbiological and epidemiological understanding of cholera outbreaks. Accurate identification and mechanistic understanding of large scale climatic, geophysical and oceanic processes governing cholera-chlorophyll relationship is important for developing cholera prediction models. Development of a holistic understanding of these processes requires long and reliable chlorophyll dataset(s), which are beginning to be available through satellites. We have presented a schematic pathway and a modeling framework that relate cholera with various hydroclimatic and oceanic variables for understanding disease dynamics using latest advances in remote sensing. Satellite data, with its unprecedented spatial and temporal coverage, have potentials to monitor coastal processes and track cholera outbreaks in endemic regions.