Ocean acidification disrupts the energy balance and impairs the health of mussels (Mytilus coruscus) by weakening their trophic interactions with microalgae and intestinal microbiome

Abstract

Despite extensive research in the last two decades, exploring the potential mechanisms underlying the sensitivity and resistance of marine organisms to ocean acidification is still imperative. Species interactions can play a role in these mechanisms, but the extent to which they modulate organismal responses to ocean acidification remains largely unknown. Here, we investigated how ocean acidification (pH 7.7) affects energy homeostasis and fitness of mussels (Mytilus coruscus) by assessing their physiological responses, intestinal microbiome and nutritional quality of their food (microalgae). Under ocean acidification, the mussels had reduced feeding rates by 34 % and reduced activities of digestive enzymes (pepsin by 39 %, trypsin by 28 % and lipase by 53 %) due to direct exposure to acidified seawater and increased phenol content of microalgae. Richness and diversity of intestinal microbiome (OTU, Chao1 index and Shannon index) were also lowered by ocean acidification, which can undermine nutrient absorption. On the other hand, energy expenditure of mussels increased by 53 % under ocean acidification, which was associated with the upregulation of antioxidant defence (SOD, CAT and GPx activities). Consequently, energy reserves in mussels decreased by 28 %, which were underpinned by the reduction in protein, carbohydrate and lipid contents. Overall, we demonstrate that ocean acidification could disrupt herbivore-algae and host-microbe interactions, thereby lowering the energy balance and impairing the health of marine organisms. This can have ramifications on the population and energy dynamics of marine communities in the acidifying ocean.