Thermal preconditioning in a reef-building coral alleviates oxidative damage through a BI-1 mediated antioxidant response

Abstract

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.

Expression plasticity regulates intraspecific variation in the acclimatization potential of a reef-building coral

“…AAA + ATPases form a large superfamily of proteins with various functions spanning from protein unfolding and degradation through DNA recombination, replication, and repair to peroxisome biogenesis 62 . Rho GTPases serve as molecular switches, transducing extracellular signals from the cell membrane inside the cell 63 , are upregulated as part of a generalized stress response 27 ,and are sensitive to free radical-mediated oxidation, modulating the cellular redox state 64 , consistent with our previous findings that improved intracellular antioxidant defense systems enhance thermal tolerance 65 . Similarly, programmed cell-death pathways (e.g., autophagy and apoptosis) are involved in coral ability to withstand heat stress without excessive bleaching 29 and can be regulated by members of both Rho GTPase and AAA + ATPase superfamilies in model organisms 66,67 .…”

Metabolomic signatures of corals thriving across extreme reef habitats reveal strategies of heat stress tolerance

“…Temperature stress treatments triggered an increase in several metabolites, and notably in relative abundance of glutamine and ornithine, known precursors to the antioxidant glutathione, which may represent increased antioxidant capacities [87][88][89]. Upregulation of genes involved in the expression of the non-enzymatic antioxidant glutathione has been found in the host tissue of P. acuta that has a higher tolerance to bleaching [90], suggesting reactive oxygen species detoxification by the host may be particularly important for maintaining stability under stress.…”

Selecting Heat-Tolerant Corals for Proactive Reef Restoration

“…Requires molecular work, may be transient, some species do not harbor diverse assemblages Potentially scalable, well-studied system, predictable tradeoffs Rowan, 2004;Berkelmans and van Oppen, 2006;Sampayo et al, 2008;Cantin et al, 2009;Cunning et al, 2016 Barshis et al, 2010;Innis et al, 2018;Mayfield et al, 2018;Majerova et al, 2020*;Williams et al, 2020*;Majerova and Drury, 2021*;Roach et al, 2021 *Indicates pre-prints available online.…”