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ABSTRACT The biological utilization of dissolved silicon (DSi) influences ocean ecology and biogeochemistry. In the deep sea, hexactinellid sponges are major DSi consumers that remain poorly understood. Their DSi consumption departs from the Michaelis-Menten kinetics of shallow-water demosponges and appears particularly maladapted to incorporating DSi from the modest concentrations typical of the modern ocean. Why did sponges not adapt to the shrinking DSi availability that followed diatom expansion some 100 to 65 million years ago? We propose that sponges incorporate DSi combining passive (aquaglyceroporins) and active (ArsB) transporters, while only active transporters (SITs) operate in diatoms and choanoflagellates. Evolution of greater silicon transport efficiency appears constrained by the additional role of aquaglyceroporins in transporting essential metalloids other than silicon. We discuss the possibility that lower energy costs may have driven replacement of ancestral SITs by less efficient aquaglyceroporins, and discuss the functional implications of conservation of aquaglyceroporin-mediated DSi utilization in vertebrates. ; ACKNOWLEDGEMENTS We thank B. MacDonald for help with logistics during sponge collection and maintenance in experimental conditions, C. Sitjà for help with sponge dry and ash weights, and M. García-Puig for video editing; F. Whoriskey and J. Pratt of the (OTN, Dalhousie University) for the collection of specimens from the OTN moorings; G. Yahel (Ruppin Academic Center) for advice when building the seawater collectors of the incubation chambers. FUNDING This research was completed mostly by funds from the SponGES H2020 grant (BG-01-2015.2, agreement number 679849-2) to M.M. and A.R. and from Fisheries and Oceans Canada Strategic Program for Ecosystem-Based Research and Advice (SPERA) and International Governance Strategy (IGS) projects awarded to L.B. and E.K. This study also benefitted from funding by a PBS grant (MINECO CTM2015-67221-R) to M.M. This study is in memory of Hans Tore ...