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.

Data Table 1 
Nitrogen and carbon isotopic ratios and enrichment levels (∆δ values above 0h background) of five individual areas of interest (AOI) in the photosymbiotic bioeroding sponge Cliona orientalis after a pulse of DO¹⁵N and DO¹³C. AOI in the outer sponge body were (I) Dinoflagellate symbionts=S, (II) Cytoplasm of dinoflagellate-hosting sponge cells=Hs and (III) nearby outer-layer mesohyl cells or intercellular areas=Mo. AOI in the inner sponge body were (IV) Choanocytes=C and (V) nearby inner-layer mesohyl cells and intercellular space=Mi. Inner-body AOI displayed in Figure 1 of the main article (1b, f and j) are marked with an asterisk (*), while outer-body AOI displayed in Figure 2 (2b, f and j) are marked with a double asterisk (**).