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Allen-Waller, L.

Publications and source records attributed to Allen-Waller, L..

4 recordsLinked to original sources

The temperate coral Astrangia poculata maintains acid-base homeostasis through heat stress

Heat stress can disrupt acid-base homeostasis in reef-building corals and other tropical cnidarians, often leading to cellular acidosis that can undermine organismal function. Temperate cnidarians experience a high degree of seasonal temperature variability, leading us to hypothesize that temperate taxa have more thermally robust pH homeostasis than their tropical relatives. To test this, we investigated how elevated temperature affects intracellular pH and calcification in the temperate coral Astrangia poculata. Clonal pairs were exposed to elevated (30{degrees}C) or control (22{degrees}C) temperatures for 17 days. Despite causing damage to host tissues and symbiont cells, elevated temperature did not affect intracellular pH or inhibit calcification in A. poculata. These responses contrast with those of tropical cnidarians, which experience cellular acidification and decreased growth during heat stress. A. poculata therefore appears to have thermally resilient cellular acid-base homeostasis mechanisms, possibly due to adaptation to large seasonal temperature variations. However, we also observed tissue damage and lower egg densities in heat-treated individuals, suggesting that increasingly severe marine heatwaves can still threaten temperate coral fitness. These results provide insight into corals nuanced adaptive capacity across latitudes and biological scales.

ecology↗

Endosymbiont strategic shifts inhibit cooperation during coral bleaching recovery

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.

ecology↗

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↗

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↗