To live or die: “Fine-tuning” adaptation revealed by systemic analyses in symbiotic bathymodiolin mussels from diverse deep-sea extreme ecosystems

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 HVs or CSs stop emission, the dramatic environmental change would pose survival risks to deep-sea organisms. Up to now, limited knowledge has been available to understand the biological responses and adaptive strategy to the extreme environments and their transition from active to extinct stage, mainly due to the technical difficulties and lack of representative organisms. In this study, bathymodiolin mussels, the dominant and successful species surviving in diverse deep-sea extreme ecosystems, were collected from active and extinct HVs (Southwest Indian Ocean) or CSs (South China Sea) via two individual cruises. The transcriptomic analysis and determination of multiple biological indexes in stress defense and metabolic systems were conducted in both gills and digestive glands of mussels, together with the metagenomic analysis of symbionts in mussels. The results revealed the ecosystem- and tissue-specific transcriptional regulation in mussels, addressing the autologous adaptations in antioxidant defense, energy utilization and key compounds (i.e. sulfur) metabolism. In detail, the successful antioxidant defense contributed to conquering the oxidative stress induced during the unavoidable metabolism of xenobiotics commonly existing in the extreme ecosystems; changes in metabolic rate functioned to handle toxic matters in different surroundings; upregulated gene expression of sulfide:quinone oxidoreductase indicated an active sulfide detoxification in mussels from HVs and active stage of HVs & CSs. 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. Taken together, a new insight was proposed that symbiotic bathymodiolin mussels would develop a “finetuning” strategy combining the autologous and heterologous regulations to fulfill the efficient and effective adaptations for successful survival. [Display omitted] •High demand for activated gene regulation confirmed huge geochemical variety among ecosystems.•Transition from active to extinct stage of cold seeps would be more severe than hydrothermal vents.•Bathymodiolin mussels relied on antioxidant defense and energy metabolism to cope with stres