Allen-Waller, L. | bioRxiv Science

bioRxiv2021

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.

ecology↗

bioRxiv2021

Marine heatwaves depress metabolic activity and impair cellular acid-base homeostasis in reef-building corals regardless of bleaching susceptibility

Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching resistant and bleaching susceptible corals throughout the 2019 marine heatwave in Hawai i, a repeat bleaching event that occurred four years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching susceptible corals had lower intracellular pH than bleaching resistant corals at the peak of bleaching for both symbiont-hosting and symbiont-free cells, indicating greater disruption of acid-base homeostasis in bleaching susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid-base regulation was significantly impaired at the cellular level even in bleaching resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid-base regulation may further exacerbate the physiological effects of climate change.

ecology↗