Introduction
Corals in the family Pocilloporidae (Cnidaria: Anthozoa: Scleractinia)
are the major reef-building corals in the Indo-Pacific Ocean (Pinzon &
LaJeunesse, 2011). Pocilloporid corals generally inhabit shallow water,
which renders them susceptible to thermal and osmotic fluctuations
(Poquita-Du et al., 2019; Schmidt-Roach, Miller, Lundgren, & Andreakis,
2014). Being representatives of the “robust corals” branch, studies on
pocilloporid corals complement our understanding derived from the
Acroporidae, the extensively studied corals in the “complex corals”
branch, about impacts of anthropogenic climate change on coral reef
ecosystems (Traylor-Knowles et al., 2011). Compared to acroporid corals,
some pocilloporids have been recognized as being relatively resistant to
environmental stresses. However, bleaching, the systematic dissociation
of symbiotic zooxanthellae from coral host, can still occur in these
corals once stresses reach critical levels (Kvitt, Rosenfeld, Zandbank,
& Tchernov, 2011). As with most stony corals, pocilloporids rely on
photosynthesis by symbiotic algae as their major energy source and
cannot live as heterotrophs for prolonged periods. Extended bleaching
can therefore cause mortaility of pocilloporid corals, even though the
stressors might not be directly lethal to the coral hosts
(Traylor-Knowles et al., 2011).
In recent decades, a novel stress response called “polyp bail-out” has
been increasingly reported in pocilloporid corals (Domart-Coulon,
Tambutté, Tambutté, & Allemand, 2004; Fordyce, Camp, & Ainsworth,
2017; Kvitt et al., 2015; Sammarco, 1982; Shapiro, Kramarsky-Winter,
Gavish, Stocker, & Vardi, 2016; Wecker et al., 2018). Unlike coral
bleaching, polyp bail-out is characterized by dissociation of coral
colonies via coenosarc degradation and detachment of zooxanthellate
polyps from the calcareous skeletons (Sammarco, 1982). In natural
environments, polyp bail-out has been reported in the Great Barrier Reef
and reefs along the Pacific coast of Costa Rica, although the triggers
are still uncertain (Sammarco, 1982; Wild et al., 2014). Under
laboratory conditions, induction of polyp bail-out has been demonstrated
with different treatments, including thermal stress, acidification, and
hyperosmosis (Domart-Coulon et al., 2004; Fordyce et al., 2017; Kvitt et
al., 2015; Serrano, Coma, Inostroza, & Serrano, 2018; Shapiro et al.,
2016; Wecker et al., 2018). As detached polyps can be maintained in
laboratory conditions for periods of weeks to months (Capel, Migotto,
Zilberberg, & Kitahara, 2014; Serrano et al., 2018; Shapiro et al.,
2016), these polyps offer a different subject material for in
situ studies of coral cellular biology and of symbiotic relationships
between corals and symbiotic algae. Moreover, since detached polyps are
thought to resettle and resume skeletogenesis under favorable
conditions, polyp bail-out can be considered as an asexual reproductive
method in stony corals and may provide an alternative approach of mass
production of coral colonies for reef restoration (Sammarco, 1982;
Shapiro et al., 2016).
Identifying signaling pathways participating in polyp bail-out can help
to develop methods to induce the response without stressing the corals,
which would facilitate survival and resettlement of detached polyps.
Furthermore, understanding molecular mechanisms underlying polyp
bail-out may help us to better understand its occurrence in nature and
its ecological significance. Recently, genomes of some pocilloporid
corals have been published (Cunning, Bay, Gillette, Baker, &
Traylor-Knowles, 2018; Voolstra et al., 2017), enabling a more thorough
understanding of this response from a molecular perspective. A recent
transcriptomic study of Pocillopora damicornis during polyp
bail-out demonstrated overexpression of many caspase-encoding genes in
concert with coenosarc degradation, supporting the hypothetical link
between polyp bail-out and tissue-specific apoptosis (Kvitt et al.,
2015; Wecker et al., 2018). In that study, it was also proposed that
proteolytic enzymes, such as cathepsins, trigger degradation of the
extracellular matrix (ECM) between coral polyps and the calcareous
skeleton, resulting in detachment of individual polyps (Wecker et al.,
2018). However, our understanding of signaling pathways activating the
apoptotic and proteolytic responses in polyp bail-out is still in its
infancy.
In the present study, we applied hyperosmotic stress to induce bail-out
in P. acuta , a species closely related to P. damicornis ,
according to recent phylogenic classifications (Johnston et al., 2017;
Schmidt-Roach et al., 2014). Based on both transcriptomic analysis and
qPCR assays, we sought to identify the signaling pathways that lead to
polyp bail-out. Results show involvement of multiple signaling pathways
in polyp bail-out, including the tumor necrosis factor (TNF) and
fibroblast growth factor (FGF) signaling pathways, which likely
independently trigger apoptotsis and ECM degradation, respectively.