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The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions.

ABSTRACT: The endosymbiosis between Symbiodinium dinoflagellates and stony corals provides the foundation of coral reef ecosystems. The survival of these ecosystems is under threat at a global scale, and better knowledge is needed to conceive strategies for mitigating future reef loss. Environmental disturbance imposing temperature, salinity, and nutrient stress can lead to the loss of the Symbiodinium partner, causing so-called coral bleaching. Some of the most thermotolerant coral-Symbiodinium associations occur in the Persian/Arabian Gulf and the Red Sea, which also represent the most saline coral habitats. We studied whether Symbiodinium alter their metabolite content in response to high-salinity environments. We found that Symbiodinium cells exposed to high salinity produced high levels of the osmolyte 2-O-glycerol-α-d-galactopyranoside (floridoside), both in vitro and in their coral host animals, thereby increasing their capacity and, putatively, the capacity of the holobiont to cope with the effects of osmotic stress in extreme environments. Given that floridoside has been previously shown to also act as an antioxidant, this osmolyte may serve a dual function: first, to serve as a compatible organic osmolyte accumulated by Symbiodinium in response to elevated salinities and, second, to counter reactive oxygen species produced as a consequence of potential salinity and heat stress.

SUBMITTER: Ochsenkuhn MA

PROVIDER: S-EPMC5559212 | biostudies-other | 2017 Aug

REPOSITORIES: biostudies-other

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Project description:Reef-building corals form a complex consortium with photosynthetic algae in the family Symbiodiniaceae and bacteria, collectively termed the coral holobiont. These bacteria are hypothesized to be involved in the stress resistance of the coral holobiont, but their functional roles remain largely elusive. Here, we show that cultured Symbiodiniaceae algae isolated from the reef-building coral Galaxea fascicularis are associated with novel bacteria affiliated with the family Flavobacteriaceae Antibiotic treatment eliminated the bacteria from cultured Symbiodiniaceae, resulting in a decreased maximum quantum yield of PSII (variable fluorescence divided by maximum fluorescence [Fv/Fm]) and an increased production of reactive oxygen species (ROS) under thermal and light stresses. We then isolated this bacterial strain, named GF1. GF1 inoculation in the antibiotic-treated Symbiodiniaceae cultures restored the Fv/Fm and reduced the ROS production. Furthermore, we found that GF1 produces the carotenoid zeaxanthin, which possesses potent antioxidant activity. Zeaxanthin supplementation to cultured Symbiodiniaceae ameliorated the Fv/Fm and ROS production, suggesting that GF1 mitigates thermal and light stresses in cultured Symbiodiniaceae via zeaxanthin production. These findings could advance our understanding of the roles of bacteria in Symbiodiniaceae and the coral holobiont, thereby contributing to the development of novel approaches toward coral protection through the use of symbiotic bacteria and their metabolites.IMPORTANCE Occupying less than 1% of the seas, coral reefs are estimated to harbor ∼25% of all marine species. However, the destruction of coral reefs has intensified in the face of global climate changes, such as rising seawater temperatures, which induce the overproduction of reactive oxygen species harmful to corals. Although reef-building corals form complex consortia with bacteria and photosynthetic endosymbiotic algae of the family Symbiodiniaceae, the functional roles of coral-associated bacteria remain largely elusive. By manipulating the Symbiodiniaceae bacterial community, we demonstrated that a bacterium that produces an antioxidant carotenoid could mitigate thermal and light stresses in cultured Symbiodiniaceae isolated from a reef-building coral. Therefore, this study illuminates the unexplored roles of coral-associated bacteria under stressful conditions.

Project description:Human impacts are causing ecosystem phase shifts from coral- to algal-dominated reef systems on a global scale. As these ecosystems undergo transition, there is an increased incidence of coral-macroalgal interactions. Mounting evidence indicates that the outcome of these interaction events is, in part, governed by microbially mediated dynamics. The allocation of available energy through different trophic levels, including the microbial food web, determines the outcome of these interactions and ultimately shapes the benthic community structure. However, little is known about the underlying thermodynamic mechanisms involved in these trophic energy transfers. This study utilizes a novel combination of methods including calorimetry, flow cytometry, and optical oxygen measurements, to provide a bioenergetic analysis of coral-macroalgal interactions in a controlled aquarium setting. We demonstrate that the energetic demands of microbial communities at the coral-algal interaction interface are higher than in the communities associated with either of the macroorganisms alone. This was evident through higher microbial power output (energy use per unit time) and lower oxygen concentrations at interaction zones compared to areas distal from the interface. Increases in microbial power output and lower oxygen concentrations were significantly correlated with the ratio of heterotrophic to autotrophic microbes but not the total microbial abundance. These results suggest that coral-algal interfaces harbor higher proportions of heterotrophic microbes that are optimizing maximal power output, as opposed to yield. This yield to power shift offers a possible thermodynamic mechanism underlying the transition from coral- to algal-dominated reef ecosystems currently being observed worldwide. As changes in the power output of an ecosystem are a significant indicator of the current state of the system, this analysis provides a novel and insightful means to quantify microbial impacts on reef health.

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The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions.

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