A multilamellar organelle for chemosymbiosis in an aplacophoran mollusc adapted to anoxic cold seep sediment

Symbiosis with chemoautotrophic bacteria has evolved in many animal lineages inhabiting reducing habitats such as hydrothermal vents, allowing these holobionts to thrive in dark biospheres. In certain cases, the symbionts have become intracellular, residing within specialised bacteriocytes. Although the integration of microbial symbionts with eukaryotic cells varies across known animals, no specialised organelle dedicated to chemosynthesis has been identified. Here, we report a mode of symbiosis where sulphur-oxidising bacteria are cultured within spherical multilamellar compartments ( ~ 12 μm) in the cold-seep aplacophoran mollusc Chaetoderma shenloong. This organelle, which we name ‘dracosphera’, is ubiquitous within the hypertrophied and intricately reticulate digestive gland of C. shenloong, which has otherwise lost most of its gut. Given that the symbionts are microaerobic and the host resides in anoxic sediments tens of centimetres below the surface, the dracosphera may minimise oxygen diffusion to the bacteria, akin to mechanisms observed in microbial diazotrophs and termite hindguts, as supported by our genomic and spatial transcriptomic analyses. Hypoxia is known to induce radical adaptations in meiofauna, exemplified by the acquisition of hydrogenosomes. Our discovery of similar adaptations in C. shenloong provides insights into the evolution of such organelles in larger animals. Animals living in the deep sea often form symbiotic partnerships with chemosynthetic bacteria. Here authors discover a multilamellar organelle in the worm-mollusc Chaetoderma shenloong containing bacteria and name it dracosphera (‘dragon ball’).