The relationship between corals and dinoflagellates of the genus is fundamental to the functioning of coral ecosystems. It has been suggested that reef corals may adapt to climate change by changing their dominant symbiont type to a more thermally tolerant one, although the capacity for such a shift is potentially hindered by the compatibility of different host-symbiont pairings. Here we combined transcriptomic and metabolomic analyses to characterize the molecular, cellular, and physiological processes that underlie this compatibility, with a particular focus on, an opportunistic, thermally tolerant symbiont that flourishes in coral tissues after bleaching events. Symbiont-free individuals of the sea anemone (commonly referred to as Aiptasia), an established model system for the study of the cnidarian-dinoflagellate symbiosis, were colonized with the "normal" (homologous) symbiont and the heterologous Analysis of the host gene and metabolite expression profiles revealed that heterologous symbionts induced an expression pattern intermediate between the typical symbiotic state and the aposymbiotic state. Furthermore, integrated pathway analysis revealed that increased catabolism of fixed carbon stores, metabolic signaling, and immune processes occurred in response to the heterologous symbiont type. Our data suggest that both nutritional provisioning and the immune response induced by the foreign "invader" are important factors in determining the capacity of corals to adapt to climate change through the establishment of novel symbioses.
Globally, reef-building corals are the most prolific producers of dimethylsulphoniopropionate (DMSP) 1,2 , a central molecule in the marine sulphur cycle and precursor of the climate-active gas dimethylsulphide 3,4 . At present, DMSP production by corals is attributed entirely to their algal endosymbiont, Symbiodinium 2 . Combining chemical, genomic and molecular approaches, we show that coral juveniles produce DMSP in the absence of algal symbionts. DMSP levels increased up to 54% over time in newly settled coral juveniles lacking algal endosymbionts, and further increases, up to 76%, were recorded when juveniles were subjected to thermal stress. We uncovered coral orthologues of two algal genes recently identified in DMSP biosynthesis, strongly indicating that corals possess the enzymatic machinery necessary for DMSP production. Our results overturn the paradigm that photosynthetic organisms are the sole biological source of DMSP, and highlight the double jeopardy represented by worldwide declining coral cover, as the potential to alleviate thermal stress through coral-produced DMSP declines correspondingly.It is widely accepted that the production of dimethylsulphoniopropionate (DMSP), a central molecule in the marine sulphur cycle, is restricted to marine algae and a few species of intertidal plants 5. Marine bacteria subsequently use DMSP as a source of sulphur and carbon and can metabolize this compound into the volatile gas dimethylsulphide (DMS) 6 , by which the largest natural flux of sulphur enters the atmosphere where it exerts considerable influence on atmospheric chemistry 7 . Despite recent controversy regarding the impact of DMS emissions on global climate 8 , DMS is probably involved in local climate regulation through its oxidation into aerosol particles that induce the formation of clouds and increase their reflectivity, thereby reducing light levels and water temperatures in the marine environment 3,4 . Concentrations of DMSP and DMS found in reef-building corals are among the highest recorded in the environment 1,2 , but it has been assumed that DMSP production derives solely from the coral's endosymbiotic microalgae Symbiodinium. Evidence that the total amounts of DMSP recorded in corals are consistently higher than levels present in Symbiodinium cells alone 9,10 raises the possibility of a cryptic source of DMSP in reef-building corals. A clear understanding of the sources of DMSP on reefs and the possible effects that global warming may have on DMSP production is paramount, given the influence that coralreef-derived sulphur emissions may have on local climates 11 . Corals in the genus Acropora are the most abundant reef-building organisms in the Indo-Pacific region 12 and, as broadcast spawners, they acquire Symbiodinium from their surrounding environment after larval development. The Symbiodinium-free larvae of this genus provide a unique opportunity to investigate Symbiodinium-independent production of DMSP in corals. Results presented here demonstrate that coral hosts (kingdom: Ani...
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