Global eco-evolutionary dynamics of pathogenic Vibrio bacteria in a changing marine environment

Abstract

Climate change is driving complex ecological changes across the world. This has implications for pathogens sensitive to environmental and ecological changes, particularly for those associated with water-borne diseases amidst a changing marine environment. However, we have little insight into how climate change impacts evolutionary responses within climate-sensitive pathogen populations, such as the emergence of dominant variants from highly variable genomic backgrounds and subsequent global dispersal. Vibrio bacteria, a group of marine pathogens causing gastroenteritis, represent a tangible example of a climate-sensitive pathogen under global expansion in response to climate change, containing the only two marine pathogens (V. cholerae and V. parahaemolyticus) that have undergone worldwide expansions and caused epidemics on a global scale. Vibrio spp. are therefore a uniquely placed species to facilitate the study of possible eco-evolutionary drivers of a marine pathogen.

This thesis identified specific knowledge gaps and created a fit-for-purpose methodological framework to facilitate exploring population-specific eco-evolutionary dynamics of climate-sensitive pathogens, combining genomic and environmental data. This interdisciplinary framework was applied to the successful global expansion of a dominant V. parahaemolyticus clone (VpST3). Evolutionary and ecological driver data were found to have potential in predicting expansion dynamics using machine learning, such as whether a specific genomic isolate would become successfully established in a particular area. This thesis focused on the success of this clone in Latin America- the first expansion identified outside its endemic region of tropical Asia- identifying a parallel emergence of a divergent population with signatures of successful adaptation to Latin America's distinct local environment. This thesis quantified the previously hypothesized role of El Niño events as marine corridors for Vibrio bacteria, finding non-linear lagged effects of increasing V. parahaemolyticus detection 3-4 months after El Niño events, and identifying a gene-level dispersal mechanism that utilises marine organisms carried by surface waters during El Niño events. This thesis then combined epidemiological and environmental data in a machine learning algorithm to forecast environmentally driven V. vulnificus infections in the USA to a 0.971 sensitivity and characterised non-linear and interacting environmental associations driving such infections.

This study provided novel insights into the understanding of global Vibrio eco-evolutionary dynamics as a response to changes in their marine environment. Potential future directions of research were identified, including the operationalisation of risk models, tracking Vibrio expansion into new regions, quantifying human exposure pathways, and the development of robust Vibrio surveillance systems to increase future predictive capacity and improve our understanding of such complex eco-evolutionary dynamics.

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Identifiers

ORCID for Amy Marie Campbell: orcid.org/0000-0003-4111-8286

ORCID for Chris Hauton: orcid.org/0000-0002-2313-4226

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