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 biospheres1. In certain instances, the symbionts have become intracellular, residing within specialised bacteriocytes2. The integration of microbial symbionts with eukaryotic cells vary across known animals; however, no specialised organelle dedicated to chemosynthesis has been identified yet2. Here, we report a mode of symbiosis where sulphur-oxidising bacteria cultured within spherical multilamellar compartments (~12 m) 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 strictly anaerobic and the host resides in anoxic sediments tens of centimetres below the surface, the dracosphera may serve to minimise oxygen diffusion to the bacteria, akin to mechanisms observed in microbial diazotrophs3 or termite hindguts4, as supported by our genomic and spatial transcriptomic analyses. Hypoxic conditions have been known to induce radical adaptations in meiofauna, exemplified by the acquisition of hydrogenosomes5. Our discovery of similarly exceptional adaptations in C. shenloong provides new insights into the evolution of such organelles also in larger animals.