Introduction
Reef building stony corals live in a mutually beneficial partnership
with photosynthetic algae that provide them with essential nutrients and
oxygen. Stressful conditions such as high temperature or oceanic
acidification lead to the disruption of symbiosis known as coral
bleaching, and eventual coral death. Climate-change related thermal mass
bleaching events have become increasingly common, affecting about 75%
of coral reefs in Hawaii and 93% of surveyed corals in Great Barrier
Reef, with over 50% mortality in some regions (Couch et al., 2017;
Hoegh-Guldberg et al., 2015). Current climate-change mitigation measures
(e.g. the Paris agreement), aiming to limit global warming to 2℃, seem
not being aggressive enough to effectively moderate impacts on coral
reefs, leaving these ecosystems under an imminent threat of collapsing
and disappearing by 2050 (Ainsworth et al., 2016; Frieler et al., 2013).
Coral reefs are of particular importance for life on Earth. They produce
atmospheric oxygen – while absorbing carbon dioxide – through their
photosynthesizing symbiotic algae, they also offer necessary shelter for
marine life, serve as nurseries for fishery species, protect coastal
regions from wave exposure and provide food for more than 3 billion
people (Vercelloni et al., 2018). The World Wildlife Fund for Nature
estimates that the range of products and services that coastal and
marine environments provide can be valued conservatively at $2.5
trillion each (Hoegh-Guldberg et al., 2015). So, not surprisingly,
searching for ways to better protect coral reefs became the kernel of
coral research all over the world.
Animals and plants are known to acclimatize to stress conditions and
several recent studies show that heat acclimatization might help corals
better withstand thermal stress and reduce the severity of coral
bleaching and mortality (Bay & Palumbi, 2015; Bellantuono,
Granados-Cifuentes, Miller, Hoegh-Guldberg, & Rodriguez-Lanetty, 2012;
Palumbi, Barshis, Traylor-Knowles, & Bay, 2014). Unfortunately, this
natural protection mechanism could be lost under future climate-change
scenarios (Ainsworth et al., 2016). One proposed solution for helping
corals withstand future climate conditions is human-assisted evolution
(Committee on Interventions to Increase the Resilience of Coral Reefs,
Ocean Studies Board, Board on Life Sciences, Division on Earth and Life
Studies, & National Academies of Sciences, Engineering, and Medicine,
2019; Oppen et al., 2017). Whether it is selective breeding, managed
relocation (assisted gene flow and migration), or genetic manipulations,
the main setback is the fundamental lack of knowledge underlying
mechanisms of coral-algal symbiosis maintenance and disruption. If we
don’t understand the mechanism of bleaching and natural
acclimatization/adaptation of corals to heat stress, we can’t
responsibly define the attributes of resilience. Reversely, with a
proper understanding of coral resilient traits and their trade-offs,
current restoration projects could be scaled up to dramatically increase
impact on coral reefs worldwide.
Despite global ecological relevance, surprisingly little is known about
the cellular and molecular mechanisms of bleaching. In general, the
observations point to two prevalent strategies involved in bleaching –
apoptosis and autophagy/symbiophagy (Downs et al., 2009; Dunn,
Schnitzler, & Weis, 2007; Kvitt, Rosenfeld, & Tchernov, 2016; Pernice
et al., 2011; Tchernov et al., 2011). These two evolutionary conserved
programmed cell death (PCD) pathways may occur independently but often
simultaneously interplay or compensate for each other (Denton & Kumar,
2019; Dunn et al., 2007). For example, key pro-survival genesBcl-2 (B-cell lymphoma 2) and BI-1 (Bax inhibitor 1)
inhibit both apoptosis and autophagy, and pro-death genes BAX (Bcl2
Associated X) and BAK (Bcl2 Antagonist/Killer) activate them (Castillo
et al., 2011; Karch et al., 2017; Xu et al., 2013).
Molecular analyses from previous bleaching experiments showed
correlation of – among others - HSP70 (heat shock protein 70), and PCD
genes Bcl-2, BI-1, BAK, and BAX expressions with bleaching, and proved
the involvement of caspases – apoptotic proteases - in the process
(Kvitt et al., 2016; Pernice et al., 2011; Tchernov et al., 2011).
Transcriptomic studies in preconditioned/acclimatized corals focused
mostly on the longer-term changes in gene expression profiles and found
differences in the expressions of e.g. heat shock family proteins, genes
involved in oxidative stress and various pleiotropic cell signaling and
transcription factors such as TNFR (tumor necrosis factor receptor) or
NFkB inhibitor (NFkBI)(Bay & Palumbi, 2015; Bellantuono et al., 2012;
Palumbi et al., 2014; Thomas et al., 2018). The early phase acute heat
stress response and the role of PCD in preconditioning and acquired
thermal resilience in corals is therefore not well understood. Moreover,
the functional analyses of particular genes in the process are missing.
In our study, we used the heat susceptible stony coral Pocillopora
acuta and we show that three-day exposure to sublethal temperature
makes it more resilient to subsequent acute thermal stress via
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 early phase of the thermal
stress. After pBcl-2 activity inhibition, preconditioned corals lose the
acquired phenotype and bleach at the same rate as non-preconditioned
corals, which determines the crucial role of pBcl-2 and programmed cell
death in coral bleaching and acclimatization. Detailed analysis points
to the involvement of autophagy/symbiophagy rather than apoptosis in the
process. Corals exposed to natural oceanic summer temperatures show
stress-induced gene expression profile similar to the experimentally
preconditioned corals which suggests that during periods with high
probability of extreme temperature events, corals can naturally increase
their resilience through alterations in cell signaling.