Differential Responses of the Coral Host and Their Algal Symbiont to Thermal Stress

William Leggat,Francois Seneca,Lubna Ukani,Tracy D Ainsworth,Kenneth Wasmund,David Yellowlees,Christian R Voolstra

doi:10.1371/journal.pone.0026687

William Leggat, Francois Seneca + Show 5 more

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https://doi.org/10.1371/journal.pone.0026687

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Abstract

The success of any symbiosis under stress conditions is dependent upon the responses of both partners to that stress. The coral symbiosis is particularly susceptible to small increases of temperature above the long term summer maxima, which leads to the phenomenon known as coral bleaching, where the intracellular dinoflagellate symbionts are expelled. Here we for the first time used quantitative PCR to simultaneously examine the gene expression response of orthologs of the coral Acropora aspera and their dinoflagellate symbiont Symbiodinium. During an experimental bleaching event significant up-regulation of genes involved in stress response (HSP90 and HSP70) and carbon metabolism (glyceraldehyde-3-phosphate dehydrogenase, α-ketoglutarate dehydrogenase, glycogen synthase and glycogen phosphorylase) from the coral host were observed. In contrast in the symbiont, HSP90 expression decreased, while HSP70 levels were increased on only one day, and only the α-ketoglutarate dehydrogenase expression levels were found to increase. In addition the changes seen in expression patterns of the coral host were much larger, up to 10.5 fold, compared to the symbiont response, which in all cases was less than 2-fold. This targeted study of the expression of key metabolic and stress genes demonstrates that the response of the coral and their symbiont vary significantly, also a response in the host transcriptome was observed prior to what has previously been thought to be the temperatures at which thermal stress events occur.

Highlights

Successful symbiotic interactions depend upon the integration of gene expression and metabolism of both the host and symbiont, including successful responses to environmental stress
Apart from visual differences in pigmentation, one of the most widely used methods for detecting the early signs of bleaching is through the use of a Pulse Amplitude Modulated Flurometer (PAM) which measures the photosynthetic capacity of photosystem II (PSII) [13]
Heat shock protein response The response of both HSP70 and HSP90 genes was determined for the coral and Symbiodinium over the course of the experiment (Figure 2a,b and 3a,b)

Summary

Introduction

Successful symbiotic interactions depend upon the integration of gene expression and metabolism of both the host and symbiont, including successful responses to environmental stress. Coral bleaching is one of the most dramatic examples of the stress induced dysfunction of a symbiosis, where the Symbiodinium are expelled from their coral host, or lose their photosynthetic pigments, in response to a variety of stressors including high [2] and low [3] temperatures, acidification [4] and disease [5]. No matter the primary cause, the thermal damage to Symbiodinium leads to the production of reactive oxygen species which, it has been proposed, damages both the symbiont and the coral host (for review see [10]) and leads to the breakdown of the symbiosis through one of a variety of cellular mechanisms [11]. It has recently been demonstrated that the host cellular response, in this case the induction of apoptosis, can be detected before visual signs of bleaching or significant changes in PSII photochemistry are noted [14,15]

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