Adaptive Feeding Strategies Facilitate Resilience of Deep-Sea Cold Seep Molluscs Confronting Climate Change

Molluscs living in dynamic deep-sea cold seep environments have evolved distinct feeding strategies for survival. Here, we present the chromosome-level genomes of two sympatric mollusc species with distinct feeding strategies, a symbiosis-dependent mussel Gigantidas haimaensis and a predatory snail Phymorhynchus buccinoides. Comparative genomic analysis revealed gene family expansions related to the bacterial component degradation (e.g., b4GalTs) in G. haimaensis, suggesting an adaptation to symbiotic life. Conversely, P. buccinoides exhibited gene family expansions associated with appetite regulation (e.g., ox2r) and the digestive system (e.g., sult1 and chst), indicating genetic modifications for deep-sea predation. Furthermore, we conducted an in situ experiment mimicking a scenario in which ocean warming and sea-level rise resulted in a mass methane leakage in deep-sea cold seeps. Interestingly, G. haimaensis increased its metabolic rate and exhibited transcriptional responses. However, P. buccinoides suppressed energy production and responses at translational and posttranslational levels, which is compatible with their distinct feeding strategies. Collectively, our results provide insights on the evolutionary basis and resilience mechanisms related to energy management, which may facilitate methane tolerance of molluscs in the deep-sea cold seeps threatened by climate change.