Phenotypic plasticity of symbiotic organ highlight deep-sea mussel as model species in monitoring fluid extinction of deep-sea methane hydrate

Methane hydrates stored in cold seeps are an important source of energy and carbon for both the endemic chemosynthetic community and humanity. However, the methane fluids may cease and even stop naturally or anthropogenically, calling for a thorough evaluation of its potential impact on the endemic species and local chemosynthetic ecosystems. As one dominant megafauna in cold seeps, some of the deep-sea mussels rely on methanotrophic endosymbionts for nutrition and therefore could serve as a promising model in monitoring the dynamic changes of methane hydrate. However, knowledge on the long-term responses of deep-sea mussels to environmental stresses induced by methane reduction and deprivation, is still lacking. Here, we set up a laboratory system and cultivated methanotrophic deep-sea mussel Gigantidas platifrons without methane supply to survey the phenotypic changes after methane deprivation. While the mussels managed to survive for >10 months after the methane deprivation, drastic changes in the metabolism, function, and development of gill tissue, and in the association with methanotrophic symbionts were observed. In detail, the mussel digested all methanotrophic endosymbionts shortly after methane deprivation for nutrition and remodeled the global metabolism of gill to conserve energy. As the methane deprivation continued, the mussel replaced its bacteriocytes with ciliated cells to support filter-feeding, which is an atavistic trait in non-symbiotic mussels. During the long-term methane deprivation assay, the mussel also retained the generation of new cells to support the phenotypic changes of gill and even promoted the activity after being transplanted back to deep-sea, showing the potential resilience after long-term methane deprivation. Evidences further highlighted the participation of symbiont sterol metabolism in regulating these processes. These results collectively show the phenotypic plasticity of deep-sea mussels and their dynamic responses to methane deprivation, providing essential information in assessing the long-term influence of methane hydrate extinction. [Display omitted] •Long-term impact of simulated methane hydrate mining is evaluated using deep-sea mussel.•Mussel hosts survived >10 months after methane deprivation and loss of symbionts.•Methane deprivation reshaped the metabolism, function and development of mussel gill.•Transplantation of decolonized mussels back to deep-sea showed potential resilience to methane deprivation.