Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event.

Julia M Diaz,Laura Weber,Amy Apprill,Tong Zhang,Colleen M Hansel,Liping Xun,Caterina Brighi,Sean Mcnally

doi:10.1038/ncomms13801

Abstract

The reactive oxygen species superoxide (O2·−) is both beneficial and detrimental to life. Within corals, superoxide may contribute to pathogen resistance but also bleaching, the loss of essential algal symbionts. Yet, the role of superoxide in coral health and physiology is not completely understood owing to a lack of direct in situ observations. By conducting field measurements of superoxide produced by corals during a bleaching event, we show substantial species-specific variation in external superoxide levels, which reflect the balance of production and degradation processes. Extracellular superoxide concentrations are independent of light, algal symbiont abundance and bleaching status, but depend on coral species and bacterial community composition. Furthermore, coral-derived superoxide concentrations ranged from levels below bulk seawater up to ∼120 nM, some of the highest superoxide concentrations observed in marine systems. Overall, these results unveil the ability of corals and/or their microbiomes to regulate superoxide in their immediate surroundings, which suggests species-specific roles of superoxide in coral health and physiology.

Highlights

The reactive oxygen species superoxide (O2 À ) is both beneficial and detrimental to life
Average superoxide concentrations measured only millimetres above coral surfaces ranged from levels below bulk seawater (M. capitata) to steady-state concentrations that were B120 normalized superoxide (nM) higher than bulk seawater (P. lobata) (Fig. 1, Supplementary Table 1)
Overall, our findings demonstrate that corals and/or their microbial epibionts regulate external superoxide levels in a species-specific manner, which suggests an important role for external superoxide in the physiology and health of the coral holobiont

Summary

Introduction

The reactive oxygen species superoxide (O2 À ) is both beneficial and detrimental to life. Coral-derived superoxide concentrations ranged from levels below bulk seawater up to B120 nM, some of the highest superoxide concentrations observed in marine systems Overall, these results unveil the ability of corals and/or their microbiomes to regulate superoxide in their immediate surroundings, which suggests species-specific roles of superoxide in coral health and physiology. Coral-derived NAD(P)H oxidoreductases putatively involved in the production of extracellular superoxide are associated with increased thermotolerance of the coral Acropora millepora[19] and resistance to pathogenic white band disease in Acropora cervicornis[20]. Given the known role of superoxide in cell signalling, differentiation and proliferation[22,23,24], growth promotion[25,26], defence[27,28,29] and acquisition of the micronutrient iron[30,31] in many macro- and microorganisms, extracellular production of superoxide may have other benefits to coral health as well. Previous research suggests that the potential origins of superoxide in the coral holobiont are diverse, and biologically controlled levels of superoxide production by corals may be an integral component of coral physiology and immune defence, as seen in higher eukaryotes[27]

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