Molecular mechanisms of sperm motility are conserved in a basal metazoan
Efficient and targeted sperm motility is essential for animal reproductive success. Studies in mammals and echinoderms have uncovered a highly conserved signaling mechanism in which sperm motility is stimulated by pH-dependent activation of the cAMP-producing enzyme soluble adenylyl cyclase (sAC). However, the presence of this pathway in basal metazoans has, until now, been unexplored. Here we found that cytoplasmic alkalinization induced a rapid burst of cAMP signaling and the full activation of motility in sperm from the reef-building coral Montipora capitata. Coral sperm expressed sAC in the flagellum, midpiece, and acrosomal regions, indicating that this molecular pH sensor may play a role in regulating mitochondrial respiration and flagellar beating. In bilaterians, sAC is a central node of a broader pH-dependent signaling pathway that alters cellular behavior in response to changes to the extracellular environment. We present transcript-level evidence that a homologous pathway is present in coral sperm, including the Na+/H+ exchanger SLC9C1, protein kinase A, and the CatSper Ca2+ channel conserved even in mammalian sperm. Our discovery of this pathway in a basal metazoan species highlights the ancient origin of the pH-sAC-cAMP signaling node in sperm physiology and suggests that it may be present in many other marine invertebrate taxa for which sperm motility mechanisms remain unexplored. These results emphasize our need to better understand the role of pH-dependent signaling in marine reproductive success, particularly as worsening ocean acidification and warming due to climate change continue to impair the physiology of corals and other marine invertebrates. Statement of significanceReef-building corals are the keystone species of the worlds most biodiverse yet threatened marine ecosystems. Corals reproduce by broadcast spawning, making the ability of their sperm to swim through the water column essential for fertilization. However, little is known about the mechanisms that regulate coral sperm motility. Here we found that elevated intracellular pH promotes the production of the second messenger cAMP in coral sperm and triggers the onset of motility. This study reveals the deep conservation of a sperm activation pathway from humans to corals, presenting the first comprehensive examination of the molecular mechanisms regulating sperm motility in an ancestral animal. These results are critical for understanding the resilience of this sensitive life stage to a changing marine environment.