Living in a hot redox soup: antioxidant defences of the hydrothermal worm Alvinella pompejana

B Genard,F Zal,E Loumaye,B Knoops,Jf Rees,P Legendre,B Marie

doi:10.3354/ab00498

Abstract

The hydrothermal Pompeii worm Alvinella pompejana lives very close to the walls of black smokers and is therefore exposed to high-temperature venting fluid containing high con- centrations of sulphides and metals. The highly aerobic metabolism of these annelids, together with these extreme physico-chemical conditions, theoretically accelerates redox processes in and around the worm, potentially increasing oxidative threat by reactive oxygen species (ROS). This prompted us to analyse activity of antioxidant enzymes in A. pompejana tissues and investigate whether they are adjusted to the endogenous production of ROS by oxidative phosphorylations and/ or to the environmental conditions. This was investigated by comparing antioxidant and metabolic enzyme activities in gills, head, body wall, pygidium and guts of A. pompejana col- lected at different vent sites of the East Pacific Rise. The antioxidant defence arsenal of A. pompe- jana is peculiar, showing very low catalase (CAT) activity and very high superoxide dismutase (SOD) activity in most tissues. It is very likely that CAT is not expressed in A. pompejana, as this haemic enzyme could be inhibited by the high sulphide concentrations prevailing in the worm's environment. A. pompejana does not compensate for the low hydrogen peroxide scavenging activity of CAT by higher glutathione peroxidase (GPX) activity levels. This latter enzyme corre- lates well with cytochrome c oxidase and citrate synthase in most tissues, suggesting that oxida- tive metabolism represents the main source of peroxides managed by GPX. On the contrary, SOD shows no correlation with any metabolic enzyme and is likely adjusted to respiration- independent ROS generation. Source variations in enzyme activities are mainly observed in the animal's gills and gut, possibly reflecting differences in the vent fluid thermal regime and/or chemistry.

Highlights

Hydrothermal vents are extreme environments in many aspects
This study indicated that glutathione peroxidase (GPX) and the very low CAT-like activities were correlated to citrate synthase (CS) and cytochrome c oxidase (COX) activities, reflecting the importance of respiration as a reactive oxygen species (ROS) source
CS, COX, LDH, GPX and superoxide dismutase (SOD) activities were detected in all tissues of Alvinella pompejana and varied by 1 order of magnitude between tissues

Summary

Introduction

High pressure, elevated temperatures, high concentrations of toxic substances, such as sulphide, metals and radioisotopes, and low pH prevail in these chemosynthesis-based ecosystems (Le Bris et al 2006, Fisher et al 2007, Demina et al in press) On theoretical grounds, these physico-chemical conditions at vents are believed to favour redox processes leading to the formation of reactive oxygen species (ROS). Sulphides and ROS can interact with transition metals, which are abundant in the surrounding waters and in animal tissues, especially in gut contents, generating damaging radicals (Halliwell & Gutteridge 1986, Adly 2010) All these factors suggest that vent animals are very likely to encounter high levels of toxic derivatives of oxygen and sulphur, but very little is known about their antioxidant defence mechanisms. A recent transcriptomic approach using cDNA from the hydrothermal worm Alvinella pompejana showed that a major part of the annotated transcripts were directly related to oxidative stress, illustrating the importance of antioxidant processes in its adaptation to its extreme environment (Gagnière at al. 2010)

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