In situ transplantation and multiple omics reveal holobiont adaptation in deep-sea mussel Gigantidas haimaensis

Deep-sea mussels Gigantidas haimaensis rely on methane-oxidizing bacteria (MOB) endosymbionts for nutrition in methane seeps, yet the molecular mechanisms enabling holobiont resilience to environmental fluctuations remain unclear. Here, we integrate a chromosome-scale genome of G. haimaensis with an in situ transplantation experiment and multi-omics analyses to investigate adaptive responses to methane limitation. Transplanting mussels to a low-methane environment for 6 days reduced MOB abundance by 30.6%. Meta-transcriptomics showed that MOB prioritized methane oxidation via upregulated pmoA/pmoB genes but downregulated amino acid biosynthesis and non-essential pathways, indicating metabolic resource reallocation. Concurrently, host transcriptomics revealed a shift from symbiont-dependent strategies (“farming” and “milking”) to filter-feeding and extracellular matrix remodeling, indicating changes in trophic level. This dynamic interplay demonstrates how the holobiont balances symbiont maintenance with alternative energy acquisition under stress and highlights the vulnerability of chemosynthetic symbioses to methane fluctuations induced by environmental changes.