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Differential responses of the coral host and their algal symbiont to thermal stress.

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, ?-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 ?-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.

SUBMITTER: Leggat W

PROVIDER: S-EPMC3200360 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Differential responses of the coral host and their algal symbiont to thermal stress.

Leggat William W Seneca Francois F Wasmund Kenneth K Ukani Lubna L Yellowlees David D Ainsworth Tracy D TD

PloS one 20111024 10

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 ...[more]

PMID: 22039532

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Project description:BackgroundCoral bleaching can be defined as the loss of symbiotic zooxanthellae and/or their photosynthetic pigments from their cnidarian host. This major disturbance of reef ecosystems is principally induced by increases in water temperature. Since the beginning of the 1980s and the onset of global climate change, this phenomenon has been occurring at increasing rates and scales, and with increasing severity. Several studies have been undertaken in the last few years to better understand the cellular and molecular mechanisms of coral bleaching but the jigsaw puzzle is far from being complete, especially concerning the early events leading to symbiosis breakdown. The aim of the present study was to find molecular actors involved early in the mechanism leading to symbiosis collapse.ResultsIn our experimental procedure, one set of Pocillopora damicornis nubbins was subjected to a gradual increase of water temperature from 28 degrees C to 32 degrees C over 15 days. A second control set kept at constant temperature (28 degrees C). The differentially expressed mRNA between the stressed states (sampled just before the onset of bleaching) and the non stressed states (control) were isolated by Suppression Subtractive Hybridization. Transcription rates of the most interesting genes (considering their putative function) were quantified by Q-RT-PCR, which revealed a significant decrease in transcription of two candidates six days before bleaching. RACE-PCR experiments showed that one of them (PdC-Lectin) contained a C-Type-Lectin domain specific for mannose. Immunolocalisation demonstrated that this host gene mediates molecular interactions between the host and the symbionts suggesting a putative role in zooxanthellae acquisition and/or sequestration. The second gene corresponds to a gene putatively involved in calcification processes (Pdcyst-rich). Its down-regulation could reflect a trade-off mechanism leading to the arrest of the mineralization process under stress.ConclusionUnder thermal stress zooxanthellae photosynthesis leads to intense oxidative stress in the two partners. This endogenous stress can lead to the perception of the symbiont as a toxic partner for the host. Consequently, we propose that the bleaching process is due in part to a decrease in zooxanthellae acquisition and/or sequestration. In addition to a new hypothesis in coral bleaching mechanisms, this study provides promising biomarkers for monitoring coral health.

Project description:BackgroundOcean warming is a leading cause of increasing episodes of coral bleaching, the dissociation between coral hosts and their dinoflagellate algal symbionts in the family Symbiodiniaceae. While the diversity and flexibility of Symbiodiniaceae is presumably responsible for variations in coral response to physical stressors such as elevated temperature, there is little data directly comparing physiological performance that accounts for symbiont identity associated with the same coral host species. Here, using Pocillopora damicornis harboring genotypically distinct Symbiodiniaceae strains, we examined the physiological responses of the coral holobiont and the dynamics of symbiont community change under thermal stress in a laboratory-controlled experiment.ResultsWe found that P. damicornis dominated with symbionts of metahaplotype D1-D4-D6 in the genus Durusdinium (i.e., PdD holobiont) was more robust to thermal stress than its counterpart with symbionts of metahaplotype C42-C1-C1b-C1c in the genus Cladocopium (i.e., PdC holobiont). Under ambient temperature, however, the thermally sensitive Cladocopium spp. exhibited higher photosynthetic efficiency and translocated more fixed carbon to the host, likely facilitating faster coral growth and calcification. Moreover, we observed a thermally induced increase in Durusdinium proportion in the PdC holobiont; however, this "symbiont shuffling" in the background was overwhelmed by the overall Cladocopium dominance, which coincided with faster coral bleaching and reduced calcification.ConclusionsThese findings support that lineage-specific symbiont dominance is a driver of distinct coral responses to thermal stress. In addition, we found that "symbiont shuffling" may begin with stress-forced, subtle changes in the rare biosphere to eventually trade off growth for increased resilience. Furthermore, the flexibility in corals' association with thermally tolerant symbiont lineages to adapt or acclimatize to future warming oceans should be viewed with conservative optimism as the current rate of environmental changes may outpace the evolutionary capabilities of corals. Video Abstract.

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Differential responses of the coral host and their algal symbiont to thermal stress.

Publications

Differential responses of the coral host and their algal symbiont to thermal stress.

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