Silicon transport in deep-water sponges deciphered: ecophysiological, evolutionary and biogeochemical implications

Avid utilization of dissolved silicon (DSi) by diatoms fuels primary productivity in the photic ocean, but how DSi is utilized at depth in the aphotic ocean, where aggregations of sponges are major DSi consumers, remains unknown. Here we present the first kinetic model of DSi consumption developed for a sponge in the class Hexactinellid, a group of sponges consisting of deep-sea specialists. The kinetics reveals surprising maladaptation, since only DSi concentrations greater than those available in contemporary oceans ensure efficient incorporation of this skeletonizing nutrient. Through a laboratory experiment associated to transcriptomic analysis, we have identified the membrane transporters involved in the Si uptake. Collaboration between passive and active Si transporters during the DSi consumption process —versus only active transporters (SITs) in diatoms and choanoflagellates— was revealed, being also interpreted as the main cause for the sponge inefficiency at low DSi concentrations. Such a poor performance at low DSi concentrations emerges as the main driver that has confined hexactinellid sponges into deep waters where DSi concentrations are comparatively higher than in shallow waters. How and why sponges replaced ancestral choanoflagellate SITs by less efficient passive transporters remains unresolved, but the functional change, conserved through animal evolution, still transports Si during bone formation in vertebrates.