Abstract

We developed and used a microsensor to measure fast (<1 s) dynamics of hydrogen peroxide (H2O2) on the polyp tissue of two scleractinian coral species (Stylophora pistillata and Pocillopora damicornis) under manipulations of illumination, photosynthesis, and feeding activity. Our real-time tracking of H2O2 concentrations on the coral tissue revealed rapid changes with peaks of up to 60 μM. We observed bursts of H2O2 release, lasting seconds to minutes, with rapid increase and decrease of surficial H2O2 levels at rates up to 15 μM s–1. We found that the H2O2 levels on the polyp surface are enhanced by oxygenic photosynthesis and feeding, whereas H2O2 bursts occurred randomly, independently from photosynthesis. Feeding resulted in a threefold increase of baseline H2O2 levels and was accompanied by H2O2 bursts, suggesting that the coral host is the source of the bursts. Our study reveals that H2O2 levels at the surface of coral polyps are much higher and more dynamic than previously reported, and that bursts are a regular feature of the H2O2 dynamics in the coral holobiont.

Highlights

  • Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2) and superoxide anion (O2·−), are toxic at high levels, and function as signaling molecules essential for the integrity of homeostasis and health of cells in most eukaryotic organisms (D’Autréaux and Toledano, 2007; Nathan and Cunningham-Bussel, 2013)

  • We developed a microsensor to measure H2O2 concentrations and applied it toward the fine-scale study of H2O2 dynamics at the surface of scleractinian coral polyps

  • The small negative values seen in our measurements suggest that the calibration regressions may be anomalous to apply to measurements made within the coral mass boundary layer (MBL), in the low range of [H2O2] values

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Summary

Introduction

Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2) and superoxide anion (O2·−), are toxic at high levels, and function as signaling molecules essential for the integrity of homeostasis and health of cells in most eukaryotic organisms (D’Autréaux and Toledano, 2007; Nathan and Cunningham-Bussel, 2013). ROS are produced under normal growth conditions, but stress conditions trigger elevated concentrations and production rates (Mittler, 2002), causing deleterious effects to vital cell organelles (Lesser, 2006). As high levels of ROS can cause oxidative damage, organisms tightly regulate internal levels of ROS through antioxidant activity of enzymes such as superoxide dismutase, catalase, and ascorbate peroxidase (Fridovich, 1998; Mittler, 2002). The occurrence of extracellular or external ROS has recently been recognized as a remarkably widespread biochemical, geochemical, and physiological pathway in marine biota and ecosystems (Sutherland et al, 2020; Hansel and Diaz, 2021).

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