Molecular mechanisms of sperm motility are conserved in an early-branching metazoan

Significance

Reef-building corals are the keystone species of the world’s most biodiverse yet threatened marine ecosystems. Coral reproduction, critical for reef resilience, requires that coral sperm swim through the water column to reach the egg. However, little is known about the mechanisms that regulate coral sperm motility. We found here that coral sperm motility is pH dependent and that activation of motility requires signaling via the pH-sensing enzyme soluble adenylyl cyclase. 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 early-diverging animal. These results are critical for understanding the resilience of this sensitive life stage to a changing marine environment.

Abstract

Efficient and targeted sperm motility is essential for animal reproductive success. Sperm from mammals and echinoderms utilize 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 early-branching metazoans has remained unexplored. Here, we found that elevating cytoplasmic pH induced a rapid burst of cAMP signaling and triggered the onset of motility in sperm from the reef-building coral Montipora capitata in a sAC-dependent manner. Expression of sAC in the mitochondrial-rich midpiece and flagellum of coral sperm support a dual role for this molecular pH sensor in regulating mitochondrial respiration and flagellar beating and thus motility. In addition, we found that additional members of the homologous signaling pathway described in echinoderms, both upstream and downstream of sAC, are expressed in coral sperm. These include the Na+/H+ exchanger SLC9C1, protein kinase A, and the CatSper Ca2+ channel conserved even in mammalian sperm. Indeed, the onset of motility corresponded with increased protein kinase A activity. Our discovery of this pathway in an early-branching 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 the need to better understand the role of pH-dependent signaling in the reproductive success of marine animals, particularly as climate change stressors continue to alter the physiology of corals and other marine invertebrates.

Speer K. F., Allen-Waller L., Novikov D. R. & Barott K. L., 2021. Molecular mechanisms of sperm motility are conserved in an early-branching metazoan. Proceedings of the National Academy of Sciences 118(48): e2109993118. doi: 10.1073/pnas.2109993118. Article.


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