Triggers, cascades, and endpoints: connecting the dots of coral bleaching mechanisms

Abstract

The intracellular coral–dinoflagellate symbiosis is the engine that underpins the success of coral reefs, one of the most diverse ecosystems on the planet. However, the breakdown of the symbiosis and the loss of the microalgal symbiont (i.e. coral bleaching) due to environmental changes are resulting in the rapid degradation of coral reefs globally. There is an urgent need to understand the cellular physiology of coral bleaching at the mechanistic level to help develop solutions to mitigate the coral reef crisis. Here, at an unprecedented scope, we present novel models that integrate putative mechanisms of coral bleaching within a common framework according to the triggers (initiators of bleaching, e.g. heat, cold, light stress, hypoxia, hyposalinity), cascades (cellular pathways, e.g. photoinhibition, unfolded protein response, nitric oxide), and endpoints (mechanisms of symbiont loss, e.g. apoptosis, necrosis, exocytosis/vomocytosis). The models are supported by direct evidence from cnidarian systems, and indirectly through comparative evolutionary analyses from non‐cnidarian systems. With this approach, new putative mechanisms have been established within and between cascades initiated by different bleaching triggers. In particular, the models provide new insights into the poorly understood connections between bleaching cascades and endpoints and highlight the role of a new mechanism of symbiont loss, i.e. ‘symbiolysosomal digestion’, which is different from symbiophagy. This review also increases the approachability of bleaching physiology for specialists and non‐specialists by mapping the vast landscape of bleaching mechanisms in an atlas of comprehensible and detailed mechanistic models. We then discuss major knowledge gaps and how future research may improve the understanding of the connections between the diverse cascade of cellular pathways and the mechanisms of symbiont loss (endpoints).

Molecular hydrogen can minimize negative effects of heat stress on the hard coral genusAcropora

“…However, simultaneous exposure to hydrogen and heat stress prevented the decline in the ETR max observed with heat stress alone in Acropora spp.. As shown in previous studies, a decrease in ETR max can serve as an indicator of damage to the photosystem and thereby a deteriorated health state of the Symbiodiniaceae cells [52,53]. This damage presumably originates from the accumulation of ROS/RNS under heat stress as proposed by the "Oxidative Theory" [20,21,22,54,55]. Our result therefore suggests that molecular hydrogen might have protected the coral holobiont against oxidative damage, thereby preventing a decrease in ETR max .…”

“…Direct actions and strategies are therefore urgently needed to further prevent the rapid degradation of these highly valuable ecosystems thereby gaining time for coral reefs until climate change becomes manageable by global efforts [18]. Shifts in physical and biogeochemical conditions are widely recognized to predominantly induce coral bleaching referring to the loss of the coral's endosymbiotic algae Symbiodiniaceae often representing the main energy source of the coral host [19,20]. Novel approaches could therefore aim to target cascades associated with coral bleaching, particularly those initiated by heat stress, offering a promising approach for intervention.…”

Coral larvae employ nitrogen sequestration mechanisms to stabilize carbon provisioning from algal symbionts under increased temperature

“…Coral bleaching occurs when the nutritional exchange of the symbiosis is disrupted, resulting in the loss of the Symbiodiniaceae, which is the coral's primary source of nutrition [13][14][15], and can result in mass mortality [11,[16][17][18]. The mechanisms underlying the onset and progression of coral bleaching are complex and a topic of intense scientific study (see a recent review in [19]). Research in the last two decades has demonstrated that oxidative stress [19,20], as well as carbon and nitrogen imbalance can drive dysbiosis and lead to bleaching [19,[21][22][23][24][25].…”

“…The mechanisms underlying the onset and progression of coral bleaching are complex and a topic of intense scientific study (see a recent review in [19]). Research in the last two decades has demonstrated that oxidative stress [19,20], as well as carbon and nitrogen imbalance can drive dysbiosis and lead to bleaching [19,[21][22][23][24][25].…”