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Marine sponges are set to become more abundant in many near-future oligotrophic environments, where they play crucial roles in nutrient cycling. Of high importance is their mass turnover of dissolved organic matter (DOM), a heterogeneous mixture that constitutes the largest fraction of organic matter in the ocean and is recycled primarily by bacterial mediation. Little is known, however, about the mechanism that enables sponges to incorporate large quantities of DOM in their nutrition, unlike most other invertebrates. Here, we examine the cellular capacity for direct processing of DOM, and the fate of the processed matter, inside a dinoflagellate-hosting bioeroding sponge that is prominent on Indo-Pacific coral reefs. Integrating transmission electron microscopy with nanoscale secondary ion mass spectrometry, we track 15N- and 13C-enriched DOM over time at the individual cell level of an intact sponge holobiont. We show initial high enrichment in the filter-feeding cells of the sponge, providing visual evidence of their capacity to process DOM through pinocytosis without mediation of resident bacteria. Subsequent enrichment of the endosymbiotic dinoflagellates also suggests sharing of host nitrogenous wastes. Our results shed light on the physiological mechanism behind the ecologically important ability of sponges to cycle DOM via the recently described sponge loop.

The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields with considerably disparate geological, physical and chemical environmental conditions. Results of population genomics analyses reveal an incongruent phylogeny between the endosymbiont and mitochondrial genomes of the scaly-foot snails in the five vent fields sampled, indicating that the hosts obtain endosymbionts via horizontal transmission in each generation. However, the genetic homogeneity of many symbiont populations implies that vertical transmission cannot be ruled out either. Fluorescence in situ hybridisation of ovarian tissue yields symbiont signals around the oocytes, suggesting that vertical transmission co-occurs with horizontal transmission. Results of in situ environmental measurements and gene expression analyses from in situ fixed samples show that the snail host buffers the differences in environmental conditions to provide the endosymbionts with a stable intracellular micro-environment, where the symbionts serve key metabolic functions and benefit from the host's cushion. The mixed transmission mode, symbiont specificity at the species level, and stable intracellular environment provided by the host support the evolutionary, ecological, and physiological success of scaly-foot snail holobionts in different vents with unique environmental parameters.