Preconditioning improves bleaching susceptibility in the reef-building coral Pocillopora acuta through modulations in autophagy pathway

Abstract

Stony corals heavily rely on their intracellular algal symbionts for energetical supply. Increasing extreme weather driven by climate change often leads to disruption of the symbiosis and to coral death, threatening the sole existence of coral reefs, the key underwater ecosystems. As climate change mitigation outcomes are uncertain, it is important to search for ways to increase coral resilience towards future climate conditions, thermal extremes in particular. It has been shown that corals can withstand stress conditions better after previous exposure, but the mechanism remains unclear. Here we show that after threeday thermal preconditioning, stony coral Pocillopora acuta becomes more resilient to acute heat stress through 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 thermal stress, and the coral bleaching rate significantly decreases. After pBcl-2 activity inhibition, preconditioned corals lose the acquired beneficial phenotype and bleach at the same rate as non-preconditioned corals, which confirms the crucial role of programmed cell death in coral bleaching and acclimatization. The detailed analysis points to the involvement of autophagy/symbiophagy rather than apoptosis in the process. A similar shift in gene expression also occurs in thermally stressed corals that have previously acclimatized to summer temperatures in Kaneohe Bay, Hawai'i, suggesting that corals can naturally increase their resilience to warming events during high-risk periods through alterations in cell signaling.An in-depth understanding of molecular mechanisms underlying coral acclimatization and resilience could open the way for restoration practices such as human-assisted evolution.

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

“…Transcriptomic studies in acclimatized corals shed light on the main gene families and cellular pathways that play a role in the bleaching process, but functional studies have been largely missing in reef-building corals (32,33,35,49). Recently, we showed that preconditioning in Pocillopora acuta leads to improved thermal tolerance due to modulations in the programmed cell death pathway (PCD), most likely via autophagy/symbiophagy (39). However, the primary signals or molecular consequences of such a prolonged symbiosis maintenance under thermal stress are unclear.…”

“…This difference was more pronounced after 5 days of heat stress. However, PC corals still lost symbionts, but significantly more slowly than in NPC corals (p< 0.001) (39).…”

“…BI-1 (BAX inhibitor 1) is an anti-apoptotic protein that -among others -promotes cell survival by increasing the production of antioxidants through the activation of Nrf2 transcription factor in human cells (42,43). We previously showed that PC corals increase the expression of pa-BI-1 during acute heat stress compared to NPC corals (39). Since these observations were made on the same set of samples as our measurements of the expression of glutathione reductase (pa-GR), we examined the correlation between the gene expressions of pa-BI-1 and pa-GR.…”

“…4). We optimized the timing between siRNA administration, the beginning of a heat stress and coral sampling to reach the most significant knock-down of pa-BI-1 during the first hours of the acute heat stress when it was most strongly overexpressed in PC corals (39). We successfully inhibited pa-BI-1 expression in 8 out of 17 corals (we set a threshold of 86% gene expression as a successful knock-down) ranging from 13% to 86% expression compared to siNTC -corals treated with control siRNA (52.02% ± 26.23, mean ± SD).…”

“…Experimental treatments followed in Majerova et al (39). Briefly, corals were fragmented and allocated into preconditioning (PC) and control (NPC) treatments and PC corals were exposed to a 29°C for 72h before returning to ambient while NPC corals were maintained at 26°C ( Fig 1A).…”