Ocean acidification drives gut microbiome changes linked to species-specific immune defence

Ocean acidification (OA) has important effects on the intrinsic phenotypic characteristics of many marine organisms. Concomitantly, OA can alter the extended phenotypes of these organisms by perturbing the structure and function of their associated microbiomes. It is unclear, however, the extent to which interactions between these levels of phenotypic change can modulate the capacity for resilience to OA. Here, we explored this theoretical framework assessing the influence of OA on intrinsic (immunological responses and energy reserve) and extrinsic (gut microbiome) phenotypic characteristics and the survival of important calcifiers, the edible oysters Crassostrea angulata and C. hongkongensis. After one-month exposure to experimental OA (pH 7.4) and control (pH 8.0) conditions, we found species-specific responses characterised by elevated stress (hemocyte apoptosis) and decreased survival in the coastal species (C. angulata) compared with the estuarine species (C. hongkongensis). Phagocytosis of hemocytes was not affected by OA but in vitro bacterial clearance capability decreased in both species. Gut microbial diversity decreased in C. angulata but not in C. hongkongensis. Overall, C. hongkongensis was capable of maintaining the homeostasis of the immune system and energy supply under OA. In contrast, C. angulata's immune function was suppressed, and the energy reserve was imbalanced, which might be attributed to the declined microbial diversity and the functional loss of essential bacteria in the guts. This study highlights a species-specific response to OA determined by genetic background and local adaptation, shedding light on the understanding of host-microbiota-environment interactions in future coastal acidification.