Photosynthetic algal symbionts of corals produce sulphur substances that are involved in the regulation of ocean temperatures. In a twist to the tale, it emerges that coral animals produce the same compounds. See Letter p.677
Coral reefs owe their success to a symbiosis between the animal host (the coral polyp) and intracellular photosynthetic dinoflagellate algae of the genus Symbiodinium, which supply up to 95% of the host's energy requirements. Symbiodinium produce abundant amounts of the sulphur compound dimethylsulphoniopropionate (DMSP) and the volatile trace sulphur gas dimethylsulphide (DMS)1,2,3 — substances that have been proposed4 to be involved in a climate-feedback cycle. On page 677 of this issue, Raina et al.5 use chemical, genomic and molecular approaches to reveal that coral polyps also produce DMSP, in the absence of their algal symbionts. This biosynthesis may help the corals to survive conditions of thermal stress, and it adds the coral polyp as a possible player in climate regulation in areas rich in reefsFootnote 1.
Reef-building corals, such as Acropora species, are prolific producers of DMSP and DMS. DMS is also formed during the breakdown of DMSP by plankton and other marine microorganisms. Raina et al. studied the larvae of Acropora corals, which lack algal symbionts when first spawned. Keeping the larvae in alga-free conditions, the researchers found that the DMSP content of the corals increased by up to 54% over time as the larvae settled and matured, suggesting that the juvenile corals were producing it themselves.
The authors then dug deep into the genomes of Acropora millepora and Acropora digitifera, looking for evolutionary evidence of DMSP synthesis. They found that two genes encoding enzymes known to be involved in DMSP synthesis in diatoms — NADPH reductase and AdoMet-dependent methyltransferase — have clear orthologues in both Acropora and Symbiodinium. This suggests that the function of these enzymes is evolutionarily conserved between diatoms, alveolates (protist organisms that include the dinoflagellates), green plants and corals.
Raina and colleagues also analysed gene-transcript levels in A. millepora and found that the gene encoding NADPH reductase was highly expressed throughout all the coral's life stages. Expression of the gene encoding the methyltransferase was high in the early stages, but decreased after the larvae settled, and remained relatively low in adult corals. NADPH reductase is used in other cellular pathways in addition to that leading to DMSP production6, which could explain why the expression levels of this enzyme are so high. By contrast, the methyltransferase is unique to the DMSP-production pathway6,7. Its high level of expression in early life stages (before the corals acquire their symbionts) is probably the reason why the authors detected such high concentrations of DMSP in coral juveniles. However, the observation that reductase levels decrease when the coral acquires Symbiodinium suggests that the large amounts of DMSP produced by the algae influence the DMSP production by the host.
When seawater temperatures and light levels are high, the symbiosis between a coral polyp and its algae can break down, such that the algae are expelled. This process, known as coral bleaching, is predicted to increase as a result of global warming. When Raina et al. subjected the alga-free juvenile corals to thermal stress of 32 °C, they found that their DMSP levels increased by up to 76% compared with unstressed animals at 27 °C. By contrast, concentrations of a DMSP-breakdown product, acrylate, decreased. Both acrylate and DMS are extremely efficient scavengers of hydroxyl radicals and other reactive oxygen species (ROS) in phytoplankton8, and levels of ROS increase during thermal stress. These results add weight to existing evidence that DMSP and its breakdown products are involved in detoxification of ROS during thermal stress in corals9. Furthermore, Raina et al. suggest that production of DMSP by polyps might help the coral to respond to thermal stress even when those conditions have resulted in the expulsion of the algal symbionts (Fig. 1).
Raina et al. conclude that corals are likely to be the exception, rather than the rule, in regard to DMSP production by marine invertebrates harbouring photosynthetic symbionts. The genus Symbiodinium is highly diverse, containing nine distinct clades and subclades that display varying thermal tolerance. Corals that experience bleaching induced by thermal stress usually display a subsequent increase in the concentration of Symbiodinium from clades with greater thermal tolerance10. It is possible that DMSP production by the host animal gives bleached corals a survival period during which more thermally tolerant symbionts can be acquired. This suggests that past periods of climate change may have led to the acquisition of this adaptive mechanism for overcoming stress.
These findings not only help us to understand how corals may respond to changing ocean temperatures, but may also contribute to our understanding of climate-feedback cycles. According to the CLAW hypothesis4, atmospheric oxidation of DMS produced by marine organisms will result in the generation of sulphate aerosols, which are the precursors of cloud-condensation nuclei. Because these nuclei attract water vapour, they can form low-level clouds, which will decrease solar radiation and thereby reduce sea surface temperatures (Fig. 1). Although this hypothesis has been disputed11, there is evidence12,13,14,15,16that enhanced levels of low cloud, and sea surface temperature regulation, occur in areas with high coral-reef biomass, such as the western Pacific. Thus, it seems plausible that reefs contribute to local climate regulation through DMSP and DMS production by both coral polyps and their symbionts. But the thermal tolerance of the coral symbiosis goes only so far, and if this is exceeded and coral cover declines — as is being seen in response to current warming trends — this regional feedback loop may shut down.
*This article and the paper under discussion5 were published online on 23 October 2013.
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About this article
Dimethylsulfonioproprionate (DMSP) content and antioxidant capacity in the host and endosymbionts of the sea anemone Entacmaea quadricolor are influenced by the host phenotype
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