Early holobiont-level divergence and adaptation across seafloor geochemical contrasts in the deep-sea squat lobster Shinkaia crosnieri.

Deep-sea hydrothermal vents and methane seeps host unique animal communities sustained by chemosynthetic symbioses, yet how biological diversification proceeds across these geochemically distinct and geographically fragmented habitats remains poorly understood. Previous studies have largely focused on either host genomic adaptation or symbiont diversity as drivers of isolation, leaving unresolved how environmental geochemistry and host-microbe associations jointly shape evolutionary trajectories in chemosynthetic ecosystems. Here, we addressed this gap by combining chromosome-level host genomics, population resequencing, and episymbiont metagenomics in the deep-sea chemosynthetic lobster Shinkaia crosnieri, a dominant species inhabiting both hydrothermal vents and methane seeps. Genomic innovations-including sensory trade-offs (vision loss versus chemosensory expansion), metabolic compensation for pigment loss, and positive selection on respiratory protein-underpin deep-sea colonization of S. crosnieri. Populations from the Okinawa Trough vent and the South China Sea seep exhibit pronounced genetic divergence, potentially driven by Pleistocene vicariance and reinforced by divergent selection across sulfur-enriched (vent) versus sulfur-depleted, methane-dominated (seep) environments. This selection target host genes involved in chemoreception and immunity, with coordinated signatures in both sequence evolution and structural variation. Crucially, holobiont-level adaptation is amplified by habitat-specific recruitment of episymbionts: sulfur-oxidizing Campylobacterales/Thiotrichales dominate vent-associated lobsters, while methanotrophic Methylococcales prevail at seep counterparts. These symbionts partition energy niches metabolically, with seep-associated communities enhancing biosynthesis of key cofactors (e.g., coenzyme Q, tetrahydrofolate). Host transporters for these nutrients are concurrently upregulated, demonstrating functional synergy. Our findings establish that diversification in extreme environments operates holobiont-wide, where geochemical gradients synergistically shape host genomic plasticity and symbiont metabolic specialization to drive early-stage divergence.