Discussion

Our data show that heat-susceptible stony coral Pocillopora acutacan become more heat stress tolerant after previous exposure to sublethal temperatures through modulations in cell signaling. In preconditioned corals, the expression of pro-survival gene pBcl-2 increases relatively to pro-death genes pBak and pBax during acute thermal stress. After pBcl-2 activity inhibition, this beneficial phenotype is lost and preconditioned corals bleach at the same rate as non-preconditioned ones. It implies direct involvement of programmed cell death pathways in coral bleaching, but due to the complexity and interconnection of these pathways, it is difficult to identify it precisely (Castillo et al., 2011; Denton & Kumar, 2019; Dunn et al., 2007; Karch et al., 2017; Xu et al., 2013). Yet, our results indicate that autophagy, not apoptosis, underlies bleaching in P. acutaduring acute heat stress. Corals activate autophagy as a part of their immune system to eliminate intracellular bacteria (Fuess, Pinzón C, Weil, Grinshpon, & Mydlarz, 2017). From this point of view, autophagy is mostly regarded as a cell rescue pathway that allows organism to get rid of pathogens and reuse autophaged cell components as a new energetic source. In the light of existing literature and our results, we hypothesize that upon acute heat stress, coral induces symbiophagy through AMPK signaling to eliminate algae producing high levels of ROS and other toxins. At the same time, it recycles algal cellular components to meet its energetic demands. This strategy of feeding on its symbionts would solve two problems at once and would allow coral to survive for prolongated time even without its symbiont. Our hypothesis is partially backed up by the recent findings showing that corals in Kaneohe Bay did not increase heterotrophic nutrition during a 2014 mass bleaching event but significantly lowered their biomass, suggesting that they could have digest symbionts and their own tissues to survive stress conditions (Wall, Ritson‐Williams, Popp, & Gates, 2019). After preconditioning, cell signalization changes, and corals slow down the bleaching rate thus extending the period of autotrophic feeding and decreasing the chances of death by starvation.
Analysis of heat stress-induced gene expression in corals naturally acclimatized to summer temperatures showed striking correlation to gene expression in experimentally preconditioned corals but not in non-preconditioned corals acclimatized to winter temperature. It suggests that such preconditioning is a natural phenomenon that serves to temporarily increase heat resilience in corals during summer, when the risk of extreme weather event increases, but is lost towards winter months.
What exactly triggers this process and what the downstream consequences of keeping the symbionts throughout hostile thermal conditions are needs to be addressed and elucidated in future experiments.
We add new pieces to the understanding of coral plasticity in responding to heat stress and their capability to acclimatize to changing conditions via preconditioning. Nevertheless, some future climate scenarios predict changes so severe that this natural mechanism could be inefficient (Ainsworth et al., 2016). Thus, it is important to search for other ways to protect coral reefs. Human-assisted evolution approach supported by technology development (e.g. CRISPR/Cas mediated genome editing made possible in corals (Cleves, Strader, Bay, Pringle, & Matz, 2018)) offers various solutions for scientists and coral restoration practitioners (Committee on Interventions to Increase the Resilience of Coral Reefs et al., 2019; Oppen et al., 2017), but without proper understanding of resilient traits and their cellular and molecular background, they have only a limited chance to succeed.