Managing mortality from vibrio infections associated with polymicrobial "Summer Mortality Syndrome" in Pacific oysters (Magallana gigas, Thunberg 1793) with a sustainably modified, lipid-dense microalgal diet

Abstract

The aquaculture industry is an essential contributor to addressing global food insecurity, with over 820 million people experiencing hunger in 2020. As traditional food supplies face limitations, the sustainable expansion of aquaculture, particularly in developing regions, is essential to meet the nutritional needs of a growing population. The Pacific oyster (Magallana gigas) is the most heavily cultivated oyster species in global aquaculture, is recognised for its ecological and economic contributions, especially in regions where land and freshwater resources are scarce. However, the sustainability of M. gigas aquaculture is threatened by disease outbreaks, particularly those caused by polymicrobial Ostreid herpesvirus-1 (OsHV-1) and Vibrio spp., leading to significant mortality events each summer. This polymicrobial infection is termed Pacific Oyster Mortality Syndrome (POMS) and is traditionally managed using broad-spectrum antibiotics and overstocking to compensate for losses, which are unsustainable. More recently, POMS has been addressed through selective breeding, intertidal preconditioning, and dietary enrichment, which improve oyster resilience and reduce mortality, while avoiding the environmental and regulatory drawbacks of conventional methods. This thesis investigates the potential to enhance the resilience of M. gigas against Vibrio infections through dietary modifications, focusing on environmentally modifying microalgal diets to increase polyunsaturated fatty acid (PUFA) content, which in turn improves the immune function of juvenile oysters when fed the lipid-dense diet. This thesis aimed to (1) evaluate the effects of microalgal diet species on Pacific oyster physiology, and (2) assess whether Vibrio coralliilyticus infection can be sustainably managed via PUFA-enhanced microalgal diets, achieved by modifying sodium nitrate (NaNO₃) concentrations in the culture medium. PUFAs, particularly eicosapentaenoic acid (EPA), docosahexaenoic acid, (DHA), arachidonic acid (AA), itaconic acid (IA), and α-linolenic acid (ALA), are fundamental in oyster immune function as they cannot be synthesised in vivo. It was hypothesised that increased PUFA in the diet would improve oyster survival when challenged with V. coralliilyticus. The research began with an exploration of the effects of single and mixed microalgal diets on Pacific oyster physiology and gene expression. It assessed the impact of diets comprising either Isochrysis galbana, Nannochloropsis spp., or a mixed diet of both species, on oyster-mass increase, tissue and shell growth, respiration rates, cell clearance and rejection, and preferential consumption of species. Gene expression analysis focused on biomineralisation and gametogenesis candidate genes. The results showed that oysters fed a single-species diet of I. galbana exhibited significantly higher tissue mass gains and a reduced allocation of resources to shell growth, as indicated by a lower Oyster Condition Index and the upregulation of the biomineralisation gene nacrein, measured by RT-qPCR. The impact of varying NaNO3 concentrations on the production of five key fatty acids-AA, IA, ALA, EPA, and DHA-in I. galbana and N. gaditana was then measured using Fourier-Transform Infrared (FTIR) spectroscopy and Gas Chromatography Mass Spectroscopy (GC-MS). The aim of this study was to determine which concentration of NaNO3 promoted the production of the five PUFAs. The results showed that decreasing NaNO3 levels in the culture media significantly altered the lipid profiles of both microalgae, with I. galbana cultured in a medium with 2.23 x 102 µmol L-1 added NaNO3 showing the highest production of AA, IA, and ALA. The potential to manipulate microalgal lipid profiles through nutrient modification alone presents a sustainable approach to improving the nutritional quality of oyster diets. Next, the physiological effects of a lipid-dense diet derived from I. galbana grown in the 2.23 x 102 µmol L-1 NaNO3 conditions were evaluated with the aim of elucidating the physiological and gene expression responses of oysters fed a “normal” and a lipid-dense I. galbana diet. The study measured oyster respiration rates, growth, and expression of immunity-related genes, where oysters fed the lipid-dense diet exhibited significantly higher respiration rates, likely due to increased energy metabolism from lipid β-oxidation. Additionally, a significant downregulation of the apoptosis-initiator gene Caspase-8 was measured, suggesting a modulation of apoptotic pathways in response to the altered lipid metabolism when the oysters were not facing infection challenge. The final chapter focused on the survival of juvenile M. gigas following V. coralliilyticus infection after being fed the lipid-dense diet. The results were promising, with no mortalities observed in either diploid or triploid oysters in the group fed the lipid-dense diet, compared to a 20% mortality rate across both ploidies fed a standard diet. This suggested that the modified microalgal diet rich in PUFAs can improve oyster survival against Vibrio infections, offering a sustainable management strategy for oyster aquaculture. Overall, this thesis presented a novel approach to managing Vibrio infections in oyster aquaculture through the dietary modification of microalgae. The findings highlight the potential of a single-species diet of I. galbana, enhanced through nutrient manipulation, to improve oyster survival to POMS. This research contributed valuable insights into the optimisation of oyster diets, with significant implications for sustainable aquaculture practices, particularly in regions where economic and technological constraints limit access to advanced disease management strategies. The proposed dietary interventions offer a cost-effective, environmentally conscious alternative to aid oyster survival, thereby contributing to the sustainable development of oyster aquaculture.

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Identifiers

ORCID for Amy Louise Lovegrove: orcid.org/0000-0002-1118-0823

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

ORCID for Tom Bibby: orcid.org/0000-0003-1743-473X

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