Abstract
BackgroundReactive oxygen species (ROS) are thought to play a major role in cell death pathways and bleaching in scleractinian corals. Direct measurements of ROS in corals are conspicuously in short supply, partly due to inherent problems with ROS quantification in cellular systems.Methodology/Principal FindingsIn this study we characterized the dynamics of the reactive oxygen species superoxide anion radical (O2 −) in the external milieu of the coral Stylophora pistillata. Using a sensitive, rapid and selective chemiluminesence-based technique, we measured extracellular superoxide production and detoxification activity of symbiont (non-bleached) and aposymbiont (bleached) corals, and of cultured Symbiodinium (from clades A and C). Bleached and non-bleached Stylophora fragments were found to produce superoxide at comparable rates of 10−11–10−9 mol O2 − mg protein−1 min−1 in the dark. In the light, a two-fold enhancement in O2 − production rates was observed in non-bleached corals, but not in bleached corals. Cultured Symbiodinium produced superoxide in the dark at a rate of . Light was found to markedly enhance O2 − production. The NADPH Oxidase inhibitor Diphenyleneiodonium chloride (DPI) strongly inhibited O2 − production by corals (and more moderately by algae), possibly suggesting an involvement of NADPH Oxidase in the process. An extracellular O2 − detoxifying activity was found for bleached and non-bleached Stylophora but not for Symbiodinium. The O2 − detoxifying activity was partially characterized and found to resemble that of the enzyme superoxide dismutase (SOD).Conclusions/SignificanceThe findings of substantial extracellular O2 − production as well as extracellular O2 − detoxifying activity may shed light on the chemical interactions between the symbiont and its host and between the coral and its environment. Superoxide production by Symbiodinium possibly implies that algal bearing corals are more susceptible to an internal build-up of O2 −, which may in turn be linked to oxidative stress mediated bleaching.
Highlights
Reactive oxygen species (ROS), consisting of the superoxide anion radical (O22), hydrogen peroxide (H2O2), the hydroxyl radical (NOH) and hydroxyl radical ion (OH2) are formed by a variety of chemical, photochemical and biological pathways in a stepwise reduction of oxygen [1]
The system configuration allows rapid superoxide detection typically within 5–10 sec from the production source, be it a filter loaded with algae, a coral contained in a flow chamber, or a test tube spiked with O22, which is essential for such a short-lived radical
Our study places a strong emphasis on developing quantitative methods for obtaining O22 production and detoxification rates in the external milieu of the coral Stylophora pistillata and cultured Symbiodinium under non-stress conditions
Summary
Reactive oxygen species (ROS), consisting of the superoxide anion radical (O22), hydrogen peroxide (H2O2), the hydroxyl radical (NOH) and hydroxyl radical ion (OH2) are formed by a variety of chemical, photochemical and biological pathways in a stepwise reduction of oxygen [1]. Superoxide (O22), a biologically common and highly reactive oxygen species which is at the heart of this research, can react with nitric oxide (NO) to form the toxic product peroxynitrite (ONOO2, [2]) or dismutate to form hydrogen peroxide (H2O2) [1]. Either the combination of H2O2 with metal ions (e.g. iron) or the breakdown of ONOO2 can produce the highly toxic hydroxyl radical (NOH) To prevent such undesired reactions the intracellular levels of superoxide are tightly regulated by the enzyme superoxide dismutase (SOD) that catalyzes the dismutation of two superoxide radicals to hydrogen peroxide and oxygen [3]. Direct measurements of ROS in corals are conspicuously in short supply, partly due to inherent problems with ROS quantification in cellular systems
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