Discovery of deep-sea acoels from a chemosynthesis-based ecosystem

Chemosynthesis-based ecosystems such as hydrothermal vents and hydrocarbon seeps harbour various endemic species, each uniquely adapted to the extreme conditions. While some species rely on obligatory relationships with bacterial symbionts for nutrient uptake, scavengers and predators also play important roles in food web dynamics in these ecosystems. Acoels, members of the phylum Xenacoelomorpha, are simple, worm-like invertebrates found in marine environments worldwide but are scarcely understood taxa. This study presents a novel genus and species of acoel from a deep-sea hydrocarbon seep off Hatsushima, Japan, Hoftherma hatsushimaensis gen. et sp. nov. Our multi-locus phylogenetic analysis revealed that the acoels are nested within Hofsteniidae, a family previously known exclusively from shallow waters. This finding suggests that at least two independent colonization events occurred in the chemosynthesis-based environments from the phylum Xenoacoelomorpha, represented by hofsteniid acoels and Xenoturbella. Previous reports of hofsteniid species from low-oxygen and sulfide-rich environments, including intertidal habitats with decomposing leaves, in addition to H. hatsushimaensis gen. et sp. nov. from a deep-sea hydrocarbon seep, imply a common ancestral adaptation to sulfide-rich ecosystems within Hofsteniidae. Moreover, the sister relationship between solenofilomorphid acoels predominating in sulfide-rich habitats indicates common ancestral adaptation to sulfide-rich ecosystems between these two families.