Sequestration of Methane by Symbiotic Deep-Sea Annelids: Ancient and Future Implications of Redefining the Seep Influence

Deep-sea methane seeps are dynamic sources of greenhouse gas production and unique habitats supporting ocean biodiversity and productivity. Most studies have emphasized environmental methane-oxidizing bacteria and archaea as important methane sinks; however, certain animals can also enrich for and host dense communities of methanotrophs. Here, we demonstrate new animal-bacterial symbioses fueled by methane, between two undescribed species of annelid (a serpulid Laminatubus and sabellid Bispira) and distinct methane-oxidizing Methylococcales bacteria within the Marine Methylotrophic Group 2. Worm tissue d¹³C values of -44‰ to -58‰ suggested methane-fueled nutrition for both annelid species. Shipboard stable isotope labelling experiments revealed active methane oxidation to dissolved inorganic carbon, as well as assimilation of ¹³C-labelled CH₄ into animal biomass. Methane-derived carbon assimilation appears to uniquely occur, at least in part, via engulfment of methanotrophic bacteria at the host epidermal surface. These tube-dwelling worms represent a new addition to the few symbiotic animal groups known to intimately associate with methane-oxidizing bacteria for nutrition, and further explain the enigmatic mass occurrence of serpulids at 150-million-year-old fossil seeps worldwide. High-resolution seafloor surveys by an autonomous underwater vehicle suggest a significant area of coverage by these symbioses, beyond that of the typical obligate seep fauna. High-resolution seafloor surveys document significant coverage by these symbioses, beyond typical obligate seep fauna. These findings uncover novel consumers of methane in the deep-sea, and by expanding the known spatial extent of methane seeps, may have important implications for deep-sea conservation.