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

Abstract

25Deep-sea methane seeps are dynamic sources of greenhouse gas production and unique 26 habitats supporting ocean biodiversity and productivity. Here, we demonstrate new 27animal-bacterial symbioses fueled by methane, between two undescribed species of 28 annelid (a serpulid Laminatubus and sabellid Bispira) and distinct methane-oxidizing 29Methylococcales bacteria. Worm tissue δ 13 C of -44‰ to -58‰ suggested methane-fueled 30 nutrition for both species and shipboard experiments revealed active assimilation of 13 C-31 labelled CH 4 into animal biomass, occurring via engulfment of methanotrophic bacteria 32 across the host epidermal surface. These worms represent a new addition to the few 33 animals known to intimately associate with methane-oxidizing bacteria, and further 34 explain their enigmatic mass occurrence at 150-million-year-old fossil seeps. High-35 resolution seafloor surveys document significant coverage by these symbioses, beyond 36 typical obligate seep fauna. These findings uncover novel consumers of methane in the 37 deep-sea, and by expanding the known spatial extent of methane seeps, may have 38 important implications for deep-sea conservation.

Molecular analyses of the gill symbiosis of the bathymodiolin mussel Gigantidas platifrons

“…ATP molecules, which serve as the universal energy currency of life, could also be utilized by the host, either by milking (translocation of nutrient from symbiont tissue to the host cells) or by farming (direct digestion of symbionts by the host) (Ponnudurai et al, 2017a;Ponnudurai et al, 2017b;Streams et al, 1997). Currently, the best-known symbiotic MOX bacteria from marine invertebrates are found within a single lineage in the Gammaproteobacteria and are related to type I methanotrophs (Jillian and Nicole, 2009), with the exception of the recently discovered fan worm-type II methanotroph association (Goffredi et al, 2020). This preference for type I methanotrophs could be because the RuMP pathway used by type I methanotrophs requires less energy and therefore, is more efficient than the serine pathway used by type II methanotrophs (Jillian and Nicole, 2009).…”