Mechanistic understanding of immunological responses of oysters to ocean acidification

Abstract

The anthropogenic activities-driven excessive emission of CO2 can be absorbed in ocean, leading to a continuously changing carbonate chemistry and declining pH of seawater. This progressive alteration is known as ocean acidification (OA). OA usually appears with other biotic and abiotic factors, such as bacterial infection, concomitantly threatening the physiology, immunity and survival of marine organisms such as edible oysters. China, as the main producer of oyster aquaculture, contributing more than 80% of global production, is particularly concerned about this emerging issue. On the other hand, oysters have developed a sophisticated hemocyte-dominated innate immune system and the ability for rapid adaptation within a few generations, which allow them to survive and thrive under the stress of environmental changes and pathogen invasion. Although it is well known that oyster immunity can perform the protective tasks of immune recognition, signalling transduction, phagocytosis and elimination of exogenous pathogens, it is unclear to what extent OA affects the immune response of parents and offspring to pathogen infection in edible oysters, and whether the oyster species from different habitats have specific levels of resistance to OA and infection. Therefore, in this thesis, I systematically and comparatively analysed two oyster species from two habitats: estuarine species Hong Kong oyster (Crassostrea hongkongensis) and coastal species Portuguese oyster (C. angulata) to investigate the effects of long-term OA on oyster immune system and the immunological responses and molecular mechanisms of Vibrio parahaemolyticus infection through three generations under OA exposure. It was found that Hong Kong oyster showed high immune resistance to OA in the first generation, but this resistance gradually decreased in the following generations. On the other hand, Portuguese oyster was vulnerable to OA at the first generation with increasing hemocyte apoptosis, deceasing phagocytosis and bacterial clearance. This adverse effect cannot be ameliorated by adaptive plasticity in the subsequent two generations, suggesting that the OA-resistant species may lose resistance after two successive generations of OA. Interestingly, the negative effects on oyster immune system and gene expression profiles were irreversible after two generations of OA, even when returning the progeny larvae back to normal conditions. Transcriptome analysis revealed that the imbalanced energy metabolism (e.g., carbohydrate metabolism) and altered immune pathways (e.g., lysosome and autophagy) under the combination of long-term OA and bacterial infection were the underpinning molecular mechanisms for the loss of resistance. This study was the first to reveal that oysters with varying initial resistance showed a convergence of immune responses after two successive generations exposed to OA, suggesting that within-generation OA experiments possibly did not fully represent the real biological responses to environmental changes. Even the species that are currently resistant may not be the ultimate winner under climate change. In addition, my research demonstrated the changes in host-pathogen relationships induced by OA, shedding light on the possible intensification of mariculture animal diseases and foodborne human-related diseases in the context of climate change.