Genomic, transcriptomic, and proteomic insights into the symbiosis of deep-sea tubeworm holobionts

Deep-sea hydrothermal vents and methane seeps are often densely populated by animals that host chemosynthetic symbiotic bacteria, but the molecular mechanisms of such host-symbiont relationship remain largely unclear. We characterized the symbiont genome of the seep-living siboglinid Paraescarpia echinospica and compared seven siboglinid-symbiont genomes. Our comparative analyses indicate that seep-living siboglinid endosymbionts have more virulence traits for establishing infections and modulating host-bacterium interaction than the vent-dwelling species, and have a high potential to resist environmental hazards. Metatranscriptome and metaproteome analyses of the Paraescarpia holobiont reveal that the symbiont is highly versatile in its energy use and efficient in carbon fixation. There is close cooperation within the holobiont in production and supply of nutrients, and the symbiont may be able to obtain nutrients from host cells using virulence factors. Moreover, the symbiont is speculated to have evolved strategies to mediate host protective immunity, resulting in weak expression of host innate immunity genes in the trophosome. Overall, our results reveal the interdependence of the tubeworm holobiont through mutual nutrient supply, a pathogen-type regulatory mechanism, and host-symbiont cooperation in energy utilization and nutrient production, which is a key adaptation allowing the tubeworm to thrive in deep-sea chemosynthetic environments.