PIRE: Advancing Global Strategies and Understanding on the Origin of Ciguatera Fish Poisoning in Tropical Oceans

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PI: Alison Robertson (University of Southern Alabama)co-PIs: Donald Anderson (Woods Hole Oceanographic Institution)Deana Erdner (University of Texas - Austin)Michael Parsons (Florida Gulf Coast University)Tyler Smith (University of the Virgin Islands)Nontechnical Abstract:Coral reef ecosystems are among the most biodiverse habitats on earth, providing societal benefits and fishery resources critical to coastal communities. A significant threat to utilizing these resources is ciguatera fish poisoning (CFP), the most prevalent non-bacterial seafood illness. CFP is caused by the consumption of reef fish that have accumulated ciguatoxins (CTXs). These potent neurotoxins are produced by microscopic algae (dinoflagellates) that live on the surfaces of aquatic plants (e.g., macroalgae, seagrasses) and enter reef food webs through the diet of herbivorous fish and invertebrates. As these toxins move through the marine food web they are structurally modified via metabolism and increase in potency. Human exposure to CTX results in rapid onset of illness and duration of 6-8 weeks. Symptoms include gastrointestinal distress, neurological dysfunction, and cardiovascular abnormalities. There are currently no effective treatments or diagnostic tests available for CFP, and no field tests feasible for pre-market surveillance of fish destined for human consumption. Despite its severity and prevalence, CFP remains an underappreciated and under-reported problem. Most CFP affects low socioeconomic groups in remote island communities who rely on local seafood for subsistence. However, fish poisonings from recreational fishing and the international seafood trade are increasing in continental areas increasing exposure in temperate regions. A major goal of this PIRE project will be to better understand the environmental conditions affecting the production of CTXs by the source organisms and to determine the fate of the toxins through the food web across geographical regions. International partners are from Hong Kong, Cuba, Norway, Canada, Scotland (UK) and Australia.Technical Abstract:While the mechanisms and environmental drivers of toxigenic phenotypes of Gambierdiscus spp. remain unknown, many other toxigenic algae live in the same community and are capable of producing toxic metabolites that can enter the food web. The identity and toxicity of these toxins are largely unknown, but their elucidation is critical to the development of monitoring approaches for public health protection of CFP. Management strategies for CFP lag far behind other seafood safety issues due to four major deficiencies: 1) the inability to easily identify and monitor for the toxigenic Gambierdiscus species and strains responsible for CFP; 2) a lack of knowledge on the toxicity and structure secondary metabolites produced by these benthic micro-algae; 3) a limited understanding of the food web dynamics and biotransformations of these metabolites; and, 4) the inability to predict when and where CFP outbreaks are most likely to occur. Based on these interlinked needs, we have developed a central hypothesis for our PIRE program: toxigenic benthic dinoflagellates produce a stable suite of secondary metabolites (meta-metabolome) allowing them to prosper in an otherwise unstable environment driven by shifts in the epiphytic flora, available substrates, and environmental conditions. Moreover, the stability and advantages gained in this meta-metabolome are universal across toxigenic genera and applicable to many (sub)tropical reef environments. This hypothesis will be tested by examining the dynamics and persistence of toxigenic Gambierdiscus in reefs around the globe to better understand the production and fate of their toxic metabolites. Hypothesis testing will comprise three research objectives: 1) Evaluate epiphyte and Gambierdiscus community diversity and macrophyte host selectivity across spatio-temporal scales and environmental gradients in coral reef ecosystems; 2) Characterize the meta-metabolome of these communities, structurally elucidate key metabolites, and develop methods to evaluate their toxicity and functional role; 3) Utilize chemical biomarkers (toxins, lipids, stable isotopes) in bio-indicator species (primary producers and consumers) and model their fate in reef food webs. To achieve these research goals we will engage in a research program with US and International partners that integrates expertise, addresses the global nature of CFP by working across hyper-endemic regions, and develops unique and lasting educational experiences for undergraduate and graduate students from the US and abroad.