Innovations in Silicon Transport Shaped the Rise of Biosilicification and Skeletal Evolution in Sponges

Sponges are the only metazoans capable of making silica skeletons through incorporation of silicic acid (dSi) from seawater, which is polymerized using silicifying proteins. Uptake involves functional cooperation between aquaglyceroporin channels (gAQP) and arsenite efflux pumps (ArsB), a dSi transport system that, surprisingly, also functions in plants. Compared to plants, the silicon selectivity filter of sponge gAQPs is shown here to have replaced hydrophilic residues with hydrophobic ones, reducing water permeation during silicon transport. Phylogenetic analyses of 201 gAQP and 161 ArsB sequences reveal that these transporters, having prokaryotic origins, were already present in ancestral sponges, preceding the emergence of silicifying proteins and fossilized silica skeletons. Through Hexactinellida diversification, the functional interdependence of gAQP and ArsB transporters shaped a remarkable coevolution via synchronized gene duplications. This coevolution was disrupted in Demospongiae, because Heteroscleromorpha demosponges acquired, via horizontal gene transfer, a microbial gAQP that partially displaced ancestral gAQPs. This acquisition and that of an autapomorphic silicifying protein (silicatein) coincided with an exceptional diversification in Heteroscleromorpha. In contrast, sponge lineages that never developed silicifying proteins (Keratosa, Verongimorpha, Calcarea) or acquired them post-Cambrian (Homoscleromorpha, Chondrilla) lost gAQP genes while retaining ArsB homologs, implying selection against a passive dSi influx for sponges lacking dSi polymerization machinery. Thus, the ability to precipitate dSi-ie forming skeleton-likely arose as an adaptive response in early askeletal sponges to the damaging, high dSi concentrations of Precambrian oceans. The evolutionary history of dSi transporters and the fossil record support that such adaptation evolved independently four times within Porifera.