A BI-1 mediated cascade improves redox homeostasis during thermal stress and prevents oxidative damage in a preconditioned reef-building coral

Global coral reef decline is driven by the breakdown of the coral-algal symbiosis during temperature stress. Corals can acclimatize to higher temperatures on intra-generational timescales, but the complex cellular processes that underlie this ability and its trade-offs are poorly understood. We show that preconditioning-based improvements in thermal tolerance in Pocillopora acuta are accompanied by host increases in glutathione reductase (GR) activity and expression, which support a reducing intracellular environment that facilitates reactive oxygen scavenging and prevents DNA damage. We found a strong correlation between GR and BI-1 (Bax-inhibitor 1) expression in heat-stressed preconditioned corals and discovered an antioxidant response element (ARE) in the GR promoter, suggesting BI-1 could regulate GR expression in corals through the Nrf2/ARE pathway. To fortify this link, we developed an siRNA-mediated gene knockdown protocol and targeted the coral BI-1 gene. BI-1 knock-down decreased glutathione reductase expression, glutathione reductase activity and increased oxidative DNA damage in heat-stressed preconditioned corals, showing that enhanced regulation of antioxidant response during acute heat stress is a key mechanism that prevents oxidative DNA damage after preconditioning. These results describe the manipulation of an important molecular cascade at the core of symbiosis maintenance under thermal stress and show that ‘induced’ symbiosis stability does not impact DNA integrity.Significance StatementCoral bleaching is a fundamental threat to reef ecosystems, but the molecular drivers of this process remain poorly understood. We show that corals pre-exposed to sublethal thermal stress gain tolerance through their ability to process reactive oxygen species, a critical cellular toxin during coral bleaching. This ability is due to overexpression of glutathione reductase, an enzyme which stabilizes the reducing environment of the cell and buffers oxidative stress. Importantly, knock-down of genes that influence glutathione reductase expression initiates a molecular cascade that leads to DNA damage, a hallmark of oxidative thermal stress in corals. This work expands our understanding of symbiosis ecology and the importance of thermal acclimatization in corals.