Characterization of a sperm motility signaling pathway in a gonochoric coral suggests conservation across sexual systems

Abstract

Many marine invertebrates liberate their gametes into the water column broadcast spawning, where fertilization hinges upon the successful activation of sperm motility. Here, we investigated the molecular mechanisms underpinning sperm motility in the broadcast spawning coral Astrangia poculata. We found that cytosolic alkalinization activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), followed by motility, in A. poculata sperm. In addition, we show for the first time in any cnidarian that sAC activity is required to activate protein kinase A (PKA) in sperm, and that PKA activity is required for the initiation of sperm motility. Ultrastructures of A. poculata sperm displayed morphological homology to other gonochoric cnidarians, and investigation of cnidarian proteomes revealed that sAC, the central signaling node in the sperm motility pathway, demonstrates broad structural and functional conservation across a diversity of cnidarian species. Ultimately, these results suggest that the role of sAC signaling in sperm motility is conserved between sperm from gonochoric and hermaphroditic corals, which is surprising given their morphological dissimilarities. This study also offers insight into the evolution of the mechanisms controlling metazoan sperm motility. Summary statementFor broadcast spawning marine invertebrates, the initiation of sperm motility is essential for fertilization. Here, we provide evidence for conservation of a sperm motility pathway across sexual systems in corals.