Abstract

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.

Highlights

  • GeoscientificModel DevelopmentM driver of the thermal breakdown of the coral-algae sym- The high productivity and extensive accretion of skeletal biosis (“coral bleaching”)

  • I consider further a retament ciation tboettwheeeenvoslculetiroancHatirnyyidasnurco(c“lerosesegfo-ybfuatihldneindsgy”m)bciootriaclsasasnodcent 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 unicellular dinoflagellateEalagarethofSthyesgteenums Symbiodinium (W“zitohoixnatnhtihsealslasoe”c)iat(iFoing,.of1t)en(mVeiSxroecnd,iceo1nn9s9co5re;tisaSotafnzloeyo,xa2n0t0h6el)

  • For the cellular bleaching mechanism outlined by Wooldridge (2009a) (Fig. 2b, Fig. 3), the dominant symbiotic response to the 1–2 ◦C temperature excursion is the predicted increase in MI and subsequent expulsion of zooxanthellae that are “stimulated” beyond the crucial growth dynamic (i.e. “autotrophic threshold”) wherein the bulk majority of photosynthetically fixed carbon is dedicated to new algal cell growth rather than transferred to the coral host

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Summary

Introduction

M driver of the thermal breakdown of the coral-algae sym- The high productivity and extensive accretion of skeletal biosis (“coral bleaching”). In essence, when a large number of zooxanthellae are expelled (per day) and subsequently produced (per day), the increased respiratory cost of this population turnover is predicted to result in a negative autotrophic energy balance (i.e. photosynthesis : respiration < 1); which in the absence of heterotrophic carbon input, progressively compromises the hosts cellular energy reserves The implications of this suggestion are intriguing, since it implies that in natural settings, the onset of the bleaching syndrome and setting of upper thermal bleaching limits are emergent attributes of the coral symbiosis that are underpinned by the characteristic growth profile of the intracellular zooxanthellae; with excessive (re)growth potential equating with reduced thermotolerance. The following essay provides a review of this evidence, and where possible, endeavours to provide insight into the design of future experiments that can more formally test the linkage

The coral-algae symbiosis: zooxanthellae cell proliferation
A2 C1 A2
The coral-algae symbiosis: thermal tolerance coupled to zooxanthellae growth
Bleaching thresholds linked to zooxanthellae MI
Improving autotrophic carbon budgets for the coral-algae symbiosis
Findings
Conclusions

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