Species-specific metabolic responses to intermittent hypoxia in marine bivalves revealed by 1H-NMR metabolomics

Fluctuations in dissolved oxygen are characteristic of coastal environments, imposing hypoxia/reoxygenation (H/R) stress that challenges the bioenergetics and redox balance of marine benthic invertebrates, often impairing their physiological performance. While adaptations to fluctuating oxygen levels are common among coastal bivalves, the metabolic regulation underlying these adaptations in species with varying hypoxia tolerances remains poorly understood. Using untargeted ¹H-NMR spectroscopy, we investigated the metabolite profiles of heart and gill tissues in three bivalve species with differing hypoxia tolerances-Crassostrea gigas, Ostrea edulis, and Arctica islandica-following severe hypoxia (24 h at <0.01 % O₂) and subsequent reoxygenation (1.5 h at 21 % O₂). Intertidal species (C. gigas and O. edulis) efficiently metabolized hypoxically accumulated succinate during recovery, while the subtidal A. islandica appeared more susceptible to reoxygenation stress, maintaining anaerobic pathways during the recovery phase. O. edulis and A. islandica showed greater reliance on anaerobic metabolism and protein catabolism under hypoxia compared to C. gigas. All three species displayed changes in the glutamate-glutamine metabolism in response to H/R stress. Interestingly, metabolic responses of the two Ostreidae species differed greatly between gill and heart tissue. This study highlights species- and tissue-specific metabolic strategies linked to habitat and lifestyle adaptations in marine bivalves, providing insights into the role of metabolic flexibility in hypoxia tolerance of these species.