Functional and microbial insights into the gill symbiosis and metal tolerance of the cold seep mussel Gigantidas haimaensis

Deep-sea cold seeps that discharge fluids rich in methane, hydrogen sulfide, and heavy metals present extreme conditions under which only a few organisms, such as deep-sea mussels, can survive. Deep-sea mussels exploit chemosynthetic energy via symbiotic microorganisms. This study compared environmental sensing and stress responses in different tissues of Gigantidas haimaensis from the Haima cold seep through transcriptome and microbiome sequencing, biochemistry index measurements and metal content assessments to decipher its adaptive mechanisms. Transcriptomic analysis revealed distinct expression patterns among three tissues, with more genes expressed in the gill. Compared to the mantle and adductor muscle, the gill had 2519 and 4508 differentially expressed genes (DEGs), respectively, while 1453 DEGs were identified between the mantle and the adductor muscle. Up-regulated DEGs in the gill were associated with symbiont acquisition, pathogen recognition, pathogen removal, symbiotic substance exchange, and oxidative stress response. Meanwhile, the gill microbiota was dominated by methanotrophic Methylomonaceae (>85 % relative abundance). Of the 13 metals analyzed, Zn, Fe, and Cu exhibited the highest concentrations. Genes associated with distinct metal-binding pathways were expressed in different tissues. The gill also showed heightened antioxidant capacity and metal accumulation, underscoring its role in the stress response. The up-regulated genes in the adductor muscle were related to muscle contraction, while in the mantle, the up-regulated protease inhibitors were linked to humoral immunity. This study demonstrates the gill's crucial functions in symbiont and pathogen regulation as well as metal stress response, thus extending our understanding of the adaptive mechanism of G. haimaensis inhabiting cold seeps.