Abstract: 

Deep-sea bathymodioline mussels dominate extreme chemosynthetic ecosystems through obligate microbial symbioses. However, the molecular mechanisms enabling these multi-partner holobionts to adapt to severe environmental fluctuations remain poorly understood. To overcome the physiological artifacts of traditional laboratory culturing, this research pioneered challenging in situ manipulations of the Gigantidas haimaensis holobiont in the Haima methane seeps. Utilizing the ROV at 1,385 meters, mussels were relocated from an active seepage zone to a methane-depleted area. This spatial transplantation induced a 6-day methane limitation. Furthermore, a high-resolution time-series experiment (5-day limitation followed by 1-day repatriation to active seeps) was conducted and integrated with chromosome-level genomics and transcriptomics. 
Genomic analyses establish that the host actively manages symbiont homeostasis in gill tissues through specialized immune regulation, lysosomal activity, and nutrient transport pathways. Under severe environmental stress, a 6-day in situ methane limitation drives the holobiont from a symbiont-reliant metabolism to compensatory host filter-feeding. Furthermore, high-resolution time-series analyses resolving transient recovery dynamics identify a decoupled "host-buffering, symbiont-tracking" division of labor. In this phase, microbial symbionts (methanotrophs and epibionts) demonstrate rapid metabolic plasticity to track environmental shifts, while the host utilizes a decentralized regulatory architecture to buffer stress. Ultimately, this work provides a foundational mechanistic framework for understanding the resilience of chemosynthetic ecosystems amidst environmental fluctuations.