Solute selectivity and functional divergence of aquaporins in reef-building corals

Abstract

Reef-building corals are increasingly threatened by environmental stressors, including ocean warming, acidification, and osmotic stress caused by fluctuations in seawater salinity, highlighting the need for a better understanding of coral physiology. However, the molecular mechanisms by which corals regulate water and solute transport remain poorly understood. To investigate the role of aquaporins (Aqps) in coral physiology, we examined the evolutionary history and transport properties of the Aqp family in reef-building corals. Comparative genomic analyses across cnidarians revealed that the nine-member core hexacorallian aqp repertoire, comprising aqp4L1.1, aqp4L1.2, aqp4L1.3, aqp4L2, aqp4L3, glp1, glp2.1, glp2.2, and aqp12L1, has been highly conserved since the common ancestor of reef-building corals and sea anemones, whereas aqp8L was consistently absent across all examined hexacorallian species. Conservation of synteny and exon-intron structures further confirmed that major components of the aqp family architecture originated deep in metazoan evolution. Functional characterization of Acropora millepora Aqp4L and Glp proteins demonstrated that most transport properties were consistent with phylogenetic predictions, with the majority of Aqp4L proteins exhibiting water-selective permeability, whereas Glp proteins transported both water and small solutes such as glycerol. Unexpectedly, Aqp4L1.2, which belongs to the water-specific aquaporin lineage, transported not only water but also glycerol, urea, and boric acid, suggesting functional co-option after gene duplication and underscoring the evolutionary flexibility of the Aqp4L lineage. These findings suggest that the hexacorallian aqp family evolved through a combination of deep evolutionary conservation and lineage-specific functional innovation, providing new insight into the molecular foundations of coral physiology.