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.

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

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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 Hawaii, 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.

Heat stress threatens the survival of symbiotic cnidarians by causing their photosymbiosis to break down in a process known as bleaching. The direct effects of temperature on cnidarian host physiology remain difficult to describe because heat stress depresses symbiont performance, leading to host stress and starvation. The symbiotic sea anemoneExaiptasia diaphanaprovides an opportune system in which to disentangle direct vs. indirect effects of heat stress on the host, since it can survive indefinitely without symbionts. Here, we tested the hypothesis that heat stress directly influences cnidarian physiology by comparing symbiotic and aposymbiotic individuals of a clonal strain ofE. diaphana. We exposed anemones to a range of temperatures (ambient, +2°C, +4°C, +6°C) for 15-18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration, and host intracellular pH (pHi). Anemones with initially high symbiont densities experienced dose-dependent symbiont loss with increasing temperature, resulting in a corresponding decline in host photosynthate accumulation. In contrast, anemones with low initial symbiont densities did not lose symbionts or assimilate less photosynthate as temperature increased, similar to the response of aposymbiotic anemones. Interestingly, pHidecreased in anemones at higher temperatures regardless of symbiont presence, cell density, or photosynthate translocation, indicating that heat stress disrupts cnidarian acid-base homeostasis independent of symbiosis dysfunction, and that acid-base regulation may be a critical point of vulnerability for hosts of this vital mutualism.

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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.

The future of coral reefs in a warming world depends on corals' ability to resist or recover from losing their photosynthetic algal endosymbionts (coral bleaching) during marine heatwaves. Heat-tolerant algal species can confer bleaching resistance by remaining in symbiosis during heat stress but tend to provide less photosynthate to the host than heat-sensitive species. Understanding this potential nutritional tradeoff is crucial for predicting coral success under climate change, but the energetic dynamics of corals hosting different algal species during bleaching recovery are poorly understood. To test how algal energetics affects coral recovery, we heat-stressed corals (Montipora capitata) hosting either heat-sensitive Cladocopium sp. or heat-tolerant Durusdinium glynni algae for two weeks, followed by a one-month recovery period. We found that while thermotolerant D. glynni regained density and photochemical efficiency faster after bleaching than Cladocopium, this algal recovery did not correspond with host physiological recovery, and D. glynni populations still contributed less photosynthate to the host relative to Cladocopium. Further, high-density algal populations of both species translocated a smaller proportion of their photosynthate than low-density populations, and corals receiving less photosynthate suffered reduced calcification rates and lower intracellular pH. This is the first evidence of a direct negative relationship between symbiont population size and 'selfishness,' and the first to establish a connection between Symbiodiniaceae carbon translocation and coral cellular homeostasis. Together, these results suggest that algal energy reallocation towards regrowth after bleaching can harm coral physiology, and that reestablishing a beneficial endosymbiosis can pose a secondary challenge for holobionts surviving stress.