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Exposure of marine life to low oxygen is accelerating worldwide via climate change and localized pollution. Mass coral bleaching and mortality have recently occurred where reefs have experienced chronic low oxygen events. However, the mechanistic basis of tolerance to oxygen levels inadequate to sustain normal functioning (i.e. hypoxia) and whether it contributes to bleaching susceptibility, remain unknown. We therefore experimentally exposed colonies of the environmentally resilient Acropora tenuis, a common reef-building coral from the Great Barrier Reef, to deoxygenation–reoxygenation stress that was aligned to their natural night–day light cycle. Specifically, the treatment involved removing the ‘night-time O2 buffer’ to challenge the inherent hypoxia thresholds. RNA-Seq analysis revealed that coral possess a complete and active hypoxia-inducible factor (HIF)-mediated hypoxia response system (HRS) homologous to other metazoans. As expected, A. tenuis exhibited bleaching resistance and showed a strong inducibility of HIF target genes in response to deoxygenation stress. We applied this same approach in parallel to a colony of Acropora selago, known to be environmnetally susceptible, which conversely exhibited a bleaching phenotype response. This phenotypic divergence of A. selago was accompanied by contrasting gene expression profiles indicative of varied effectiveness of their HIF-HRS. Based on our RNA-Seq analysis, we propose (a) that the HIF-HRS is central for corals to manage deoxygenation stress and (b) that key genes of this system (and the wider gene network) may contribute to variation in coral bleaching susceptibility. Our analysis suggests that heat shock protein (hsp) 70 and 90 are important for low oxygen stress tolerance and further highlights how hsp90 expression might also affect the inducibility of coral HIF-HRS in overcoming a metabolic crisis under deoxygenation stress. We propose that differences in coral HIF-HRS could be central in regulating sensitivity to other climate change stressors—notably thermal stress—that commonly drive bleaching.

Summary Coral bleaching, caused by the loss of brownish-colored dinoflagellate photosymbionts from the host tissue of reef-building corals, is a major threat to reef survival. Occasionally, bleached corals become exceptionally colorful rather than white. These colors derive from photoprotective green fluorescent protein (GFP)-like pigments produced by the coral host. There is currently no consensus regarding what causes colorful bleaching events and what the consequences for the corals are. Here, we document that colorful bleaching events are a recurring phenomenon in reef regions around the globe. Our analysis of temperature conditions associated with colorful bleaching events suggests that corals develop extreme coloration within 2 to 3 weeks after exposure to mild or temporary heat stress. We demonstrate that the increase of light fluxes in symbiont-depleted tissue promoted by reflection of the incident light from the coral skeleton induces strong expression of the photoprotective coral host pigments. We describe an optical feedback loop involving both partners of the association, discussing that the mitigation of light stress offered by host pigments could facilitate recolonization of bleached tissue by symbionts. Our data indicate that colorful bleaching has the potential to identify local environmental factors, such as nutrient stress, that can exacerbate the impact of elevated temperatures on corals, to indicate the severity of heat stress experienced by corals and to gauge their post-stress recovery potential. Video Abstract Download : Download video (160MB)