Ecological diversification reveals routes of pathogen emergence in endemic Vibrio vulnificus populations

Abstract

Pathogen emergence is a complex phenomenon that, despite its public health relevance, remains poorly understood. Vibrio vulnificus, an emergent human pathogen, can cause a deadly septicaemia with over 50% mortality rate. To date, the ecological drivers that lead to the emergence of clinical strains and the unique genetic traits that allow these clones to colonize the human host remain mostly unknown. We recently surveyed a large estuary in eastern Florida, where outbreaks of the disease frequently occur, and found endemic populations of the bacterium. We established two sampling sites and observed strong correlations between location and pathogenic potential. One site is significantly enriched with strains that belong to one phylogenomic cluster (C1) in which the majority of clinical strains belong. Interestingly, strains isolated from this site exhibit phenotypic traits associated with clinical outcomes, whereas strains from the second site belong to a cluster that rarely causes disease in humans (C2). Analyses of C1 genomes indicate unique genetic markers in the form of clinical-associated alleles with a potential role in virulence. Finally, metagenomic and physicochemical analyses of the sampling sites indicate that this marked cluster distribution and genetic traits are strongly associated with distinct biotic and abiotic factors (e.g., salinity, nutrients, or biodiversity), revealing how ecosystems generate selective pressures that facilitate the emergence of specific strains with pathogenic potential in a population. This knowledge can be applied to assess the risk of pathogen emergence from environmental sources and integrated toward the development of novel strategies for the prevention of future outbreaks.

Patterns of air pressure, wind speed, and temperature are correlated with an increased risk of clinical infection from Vibrio vulnificus in endemic areas

“…Other environmental variables not measured in this analysis, such as pH and salinity, may contribute to the explanatory variance in a logistic model [55, 56]. Indeed, these highly significant variables, including rainfall events, have been reviewed in-depth in the literature as they relate to V. vulnificus and related Vibrio species [22, 57, 58].…”

“…As first proposed in the introduction, these are related to factors associated with Vibrio populations in other contexts. Rather than analyze correlations between all available NOAA environment variables, our approach was more directed and hypothesis-driven, utilizing only those meteorological measurements that we believe might have a relationship with Vibrio populations [22]. Below we describe the variables.…”

“…A study of four coastal habitats found that elevated sea surface temperatures and suspended particulate matter were variables that were predictive for detecting V. vulnificus both in water samples and oysters [21]. López-Pérez et al (2021) reported recovering V. vulnificus in Florida more often during months when the water temperature exceeded 20°C [22]. With respect to seasonality, significant fluctuations were detected in the abundance of V. vulnificus in several aquatic organisms across several Gulf states [23, 24].…”

“…With respect to seasonality, significant fluctuations were detected in the abundance of V. vulnificus in several aquatic organisms across several Gulf states [23, 24]. Thus, we cannot overstate the importance of water and ambient air temperature to the ecology of V. vulnificus [22, 25]. That said, there remain many other abiotic factors which may contribute to V. vulnificus emergence that may contribute to poor clinical outcomes.…”

When Vibrios Take Flight: A Meta-analysis of Pathogenic Vibrios Species in Wild and Domestic Birds

“…For example, Vibrio vulnificus is a causative agent of primary septicemia with a case fatality rate of up to fifty percent [27,28]. As one of world's leading causes of seafood-related deaths, Vibrio vulnificus is an opportunistic pathogen which causes high morbidity and mortality among the immunocompromised and those with liver disease [29,30]. Vibrio cholerae, specifically serotypes O1 and O139, is likely the most well-known member of the Vibrio genus.…”