Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA.
Department of Biological Sciences, University of Rhode Island, Kingston, RI 02881, USA.
Proc Biol Sci. 2023 Aug 9;290(2004):20230085. doi: 10.1098/rspb.2023.0085. Epub 2023 Aug 2.
Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signalling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric, broadcast spawning coral . We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity leads to protein kinase A (PKA) activation, and that PKA activity contributes to sperm motility activation. Ultrastructures of sperm displayed morphological homology with other gonochoric cnidarians, and sAC exhibited broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-cAMP-PKA signalling in sperm motility across coral sexual systems, and suggest that the role of this pathway in sperm motility may be ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification.
大多数石珊瑚通过广播式产卵将配子释放到水柱中,受精取决于定向精子运动的激活。雌雄异体和雌雄同体珊瑚的精子表现出明显的形态和分子表型,但尚不清楚控制精子运动的信号通路在这些性系统之间是否也不同。在这里,我们使用雌雄异体、广播式产卵的珊瑚 来解决这一知识空白。我们发现精子的细胞质碱化激活了 pH 感应酶可溶性腺苷酸环化酶 (sAC),这是运动所必需的。此外,我们首次在任何刺胞动物中证明,sAC 活性导致蛋白激酶 A (PKA) 的激活,而 PKA 活性有助于精子运动的激活。精子的超微结构显示与其他雌雄异体刺胞动物具有形态同源性,并且 sAC 在整个门中表现出广泛的结构和功能保守性。这些结果表明 pH 依赖性 sAC-cAMP-PKA 信号通路在珊瑚性系统中的精子运动中具有保守作用,并表明该途径在精子运动中的作用可能在后生动物中是祖先的。最后,这种 pH 敏感途径的动态可能在决定海洋无脊椎动物繁殖对人为海洋酸化的敏感性方面起着关键作用。