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Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals.

ABSTRACT: Over the past three decades, massive bleaching events of zooxanthellate corals have been documented across the range of global distribution. Although the phenomenon is correlated with relatively small increases in sea-surface temperature and enhanced light intensity, the underlying physiological mechanism remains unknown. In this article we demonstrate that thylakoid membrane lipid composition is a key determinate of thermal-stress sensitivity in symbiotic algae of cnidarians. Analyses of thylakoid membranes reveal that the critical threshold temperature separating thermally tolerant from sensitive species of zooxanthellae is determined by the saturation of the lipids. The lipid composition is potentially diagnostic of the differential nature of thermally induced bleaching found in scleractinian corals. Measurements of variable chlorophyll fluorescence kinetic transients indicate that thermally damaged membranes are energetically uncoupled but remain capable of splitting water. Consequently, a fraction of the photosynthetically produced oxygen is reduced by photosystem I through the Mehler reaction to form reactive oxygen species, which rapidly accumulate at high irradiance levels and trigger death and expulsion of the endosymbiotic algae. Differential sensitivity to thermal stress among the various species of Symbiodinium seems to be distributed across all clades. A clocked molecular phylogenetic analysis suggests that the evolutionary history of symbiotic algae in cnidarians selected for a reduced tolerance to elevated temperatures in the latter portion of the Cenozoic.

SUBMITTER: Tchernov D

PROVIDER: S-EPMC518791 | biostudies-literature | 2004 Sep

REPOSITORIES: biostudies-literature

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Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals.

Tchernov Dan D Gorbunov Maxim Y MY de Vargas Colomban C Narayan Yadav Swati S Milligan Allen J AJ Häggblom Max M Falkowski Paul G PG

Proceedings of the National Academy of Sciences of the United States of America 20040830 37

Over the past three decades, massive bleaching events of zooxanthellate corals have been documented across the range of global distribution. Although the phenomenon is correlated with relatively small increases in sea-surface temperature and enhanced light intensity, the underlying physiological mechanism remains unknown. In this article we demonstrate that thylakoid membrane lipid composition is a key determinate of thermal-stress sensitivity in symbiotic algae of cnidarians. Analyses of thylak ...[more]

PMID: 15340154

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Project description:Reef-building corals form an obligate symbiosis with photosynthetic microalgae in the family Symbiodiniaceae that meet most of their energy requirements. This symbiosis is under threat from the unprecedented rate of ocean warming as well as the simultaneous pressure of local stressors such as poor water quality. Only 1°C above mean summer sea surface temperatures (SSTs) on the Great Barrier Reef (GBR) can trigger the loss of Symbiodiniaceae from the host, and very low concentrations of the most common herbicide, diuron, can disrupt the photosynthetic activity of microalgae. In an era of rapid environmental change, investigation into the assisted evolution of the coral holobiont is underway in an effort to enhance the resilience of corals. Apicomplexan-like microalgae were discovered in 2008 and the Phylum Chromerida (chromerids) was created. Chromerids have been isolated from corals and contain a functional photosynthetic plastid. Their discovery therefore opens a new avenue of research into the use of alternative/additional photosymbionts of corals. However, only two studies to-date have investigated the symbiotic nature of Chromera velia with corals and thus little is known about the coral-chromerid relationship. Furthermore, the response of chromerids to environmental stressors has not been examined. Here we tested the performance of four chromerid strains and the common dinoflagellate symbiont Cladocopium goreaui (formerly Symbiodinium goreaui, ITS2 type C1) in response to elevated temperature, diuron and their combined exposure. Three of the four chromerid strains exhibited high thermal tolerances and two strains showed exceptional herbicide tolerances, greater than observed for any photosynthetic microalgae, including C. goreaui. We also investigated the onset of symbiosis between the chromerids and larvae of two common GBR coral species under ambient and stress conditions. Levels of colonization of coral larvae with the chromerid strains were low compared to colonization with C. goreaui. We did not observe any overall negative or positive larval fitness effects of the inoculation with chromerid algae vs. C. goreaui. However, we cannot exclude the possibility that chromerid algae may have more important roles in later coral life stages and recommend this be the focus of future studies.

Project description:In 2016, global temperatures were the highest on record, and mass coral bleaching occurred world-wide. However, around Sesoko Island, Okinawa, southwestern Japan, the heat stress assessed by degree heating week (DHW) based on local temperature measurements was moderate in 2016; in 1998, DHW was three times higher than in 2016 (10.6 vs. 3.3 in September in respective years). On a reef flat of Sesoko Island where the effect of severe coral bleaching on coral assemblage was monitored in 1998, significant coral bleaching occurred in 2016. Bleaching of the heat stress sensitive Acropora corals began in July 2016 on the reef flat as seawater temperature rose. We observed the bleaching and post-bleaching mortality status of individual colonies of Acropora spp. in 2016 in fixed plots on the reef flat. In total, 123 Acropora colonies were followed for six months after seawater temperature became normal by multiple surveys. At the beginning of September 2016, 99.2% of colonies, were either completely (92.7%) or partially (6.5%) bleached. Of those, the dominant species or species groups were A. gemmifera (Ag), A. digitifera (Ad), and tabular Acropora (tA). For all Acropora colonies, the overall whole and partial mortality was 41.5% and 11.4%, respectively. Whole mortality rate differed significantly among species; 72.5%, 17.9%, and 27.8% in Ag, Ad, and tA, respectively. Mortality rates at the end of the surveys were similar in smaller (?10 cm in diameter) and larger Ag, but the former suffered mortality earlier than the latter. Higher survival of smaller colonies was observed only in tA (100%), which may be associated with large morphological differences between smaller and larger colonies. Some of the dominant Acropora colonies had survived without partial mortality including 15.0% survival of the most vulnerable Ag at the end of the surveys. These results suggest that moderate heat stress may have a potential for selecting heat-tolerant genotypes. A longer period of mortality lasting for six months, was observed in Ag in addition to immediate whole mortality after bleaching, due to the continuous loss of living tissue by partial mortality. This highlights the need for multiple surveys at least during several months to accurately assess the impact of thermal stress event to corals. In contrast to DHW based on local measurements, DHW obtained from satellite data were similar between 1998 and 2016. Although satellite-based measurement of sea surface temperature is very useful to reveal variations in heat stress at a large spatial scale, temperature should be measured on site when variations at smaller spatial scales are of interest.

Dataset Information

Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals.

Publications

Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals.

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