Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae

Abstract. Impairment of the photosynthetic machinery of the algal endosymbiont ("zooxanthellae") is the proximal driver of the thermal breakdown of the coral-algae symbiosis ("coral bleaching"). Yet, the initial site of damage, and early dynamics of the impairment are still not well resolved. In this perspective essay, I consider further a recent hypothesis which proposes an energetic disruption to the carbon-concentrating mechanisms (CCMs) of the coral host, and the resultant onset of CO₂-limitation within the photosynthetic "dark reactions" as a unifying cellular mechanism. The hypothesis identifies the enhanced retention of photosynthetic carbon for zooxanthellae (re)growth following an initial irradiance-driven expulsion event as a strong contributing cause of the energetic disruption. If true, then it implies that the onset of the bleaching syndrome and setting of upper thermal bleaching limits are emergent attributes of the coral symbiosis that are ultimately underpinned by the characteristic growth profile of the intracellular zooxanthellae; which is known to depend not just on temperature, but also external (seawater) nutrient availability and zooxanthellae genotype. Here, I review this proposed bleaching linkage at a variety of observational scales, and find it to be parsimonious with the available evidence. Future experiments are suggested that can more formally test the linkage. If correct, the new cellular model delivers a valuable new perspective to consider the future prospects of the coral symbiosis in an era of rapid environmental change, including: (i) the underpinning mechanics (and biological significance) of observed changes in resident zooxanthellae genotypes, and (ii) the now crucial importance of reef water quality in co-determining thermal bleaching resistance.