Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter

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.