Systemic comparisons of the adaptations in symbiotic bathymodiolin mussels from diverse stages of hydrothermal vents and cold seeps

Hydrothermal vents (HVs) and cold seeps (CSs) are typical deep-sea extreme ecosystems with their own geochemical characteristics to supply the unique living conditions for local communities. Once the fluid vents stop emission, the dramatically environmental change would pose survival risks to deep-sea organisms and further shape the whole ecosystems. Up to now, limited knowledge was available to understand the biological responses and adaptive strategies to these extreme environments and their dual-state from active to extinct stage. In this study, bathymodiolin mussels, the dominant and successful species surviving in diverse deep-sea extreme ecosystems, were sampled from active and extinct HVs (Southwest Indian Ocean) or CSs (South China Sea) via two individual cruises. The transcriptomic analysis, determination of multiple biological indexes in stress defense and metabolic systems were conducted in both gill and digestive gland of mussels, together with the metagenomic analysis of symbionts in mussels. The results revealed the fluid-specific transcriptional regulation in mussels, addressing the autologous adaptations in successful antioxidant defense, varied energy utilization and key compounds (i.e. sulfur) metabolism due to distinction in different fluid environments. Coordinately, a heterologous adaptation, characterized by the functional compensation between symbionts and mussels in energy utilization, sulfur and carbon metabolism, was also evidenced by the bacterial metagenomic analysis in these chemosynthetic ecosystems. Taken together, a new insight was proposed that the dual-state of fluid vents drives symbiotic bathymodiolin mussels to develop an autologous and heterologous combined adaptation for successful survival.