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

Abstract

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.

Evidence for evolutionary adaptation of mixotrophic nanoflagellates to warmer temperatures

“…In general, evolved metabolic rates shifted back towards ancestral rates as they adapted, suggesting a recovery from stress-induced dysregulation to homeostasis. Stress has been shown to cause physiological and metabolic dysregulation in marine organisms (Fernández-Pinos et al 2017, Innis et al 2021. In our experiment, when mixotrophs were briefly acclimated to new thermal environments, they exhibited similar dysregulation of metabolism (either increases or decreases in metabolic rates relative to the 24 °C control lineages; Fig.…”

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

“…Sperm in particular are acutely susceptible to environmental disturbances due to their small size and brief lifespan (13), and climate change stressors including ocean warming and acidification have reduced coral sperm production (11,14), motility (10,15,16), and fertilization success (17,18) in several species. The mechanisms driving these declines in sperm performance are unknown, but both warming and acidification may disrupt coral cellular metabolism and acidify the cytosol (19)(20)(21), two processes that are important for sperm motility in other species (22). Indeed, initial evidence indicates that alkalinization of coral sperm cytosol promotes motility (23), highlighting the importance of understanding the Significance Reef-building corals are the keystone species of the world's most biodiverse yet threatened marine ecosystems.…”