Multi-omics analyses of the Alviniconcha holobiont reveal multi-faceted adaptations to deep-sea hydrothermal vents.

Deep-sea hydrothermal vents are "extreme" environments with constantly fluctuating physicochemical conditions, but dense animal aggregations thrive primarily through symbiosis with chemoautotrophic bacteria to exploit the unusual chemistry. Alviniconcha snails, which harbor symbionts in their enlarged gill at an intermediate state between intracellular and extracellular, are a prime example. Here, we present chromosome-level genomes of two Alviniconcha species (A. adamantis and A. marisindica) to investigate the adaptations of this holobiont. Significant expansion of solute carrier families enhances nutrient transport between the two parties. Alviniconcha lacks complete methionine biosynthesis pathways, likely compensated by symbiont provisioning, highlighting host-symbiont metabolic complementarity. High myoglobin expression levels in the gills contradict previous reports of hemoglobin, suggesting myoglobin-mediated oxygen storage to mitigate fluctuating environmental oxygen levels. Spatial transcriptomics further delineated gill's functional zones on the gill filament responsible for symbiont digestion via phagocytosis in bacteriocytes, oxygen transport in secretory zones, and ciliary water flow regulation. Our findings elucidate molecular and physiological adaptations underpinning the Alviniconcha holobiont's success in dynamic vent ecosystems.