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.