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

Abstract

T his authors' personal cop y m ay not be publicly o r syste m a tica lly copied or distributed, o r posted on the O pen W eb, exce pt w ith w ritten perm ission o f th e co p yrig h t holder(s). It m ay be distributed to interested individuals on request. ABSTRACT: The hydrotherm al Pompeii worm Alvinella pom pejana lives very close to the walls of black smokers and is therefore exposed to high-tem perature venting fluid containing high con centrations of sulphides and metals. The highly aerobic m etabolism of these annelids, together with these extrem e physico-chemical conditions, theoretically accelerates redox processes in and around the worm, potentially increasing oxidative threat by reactive oxygen species (ROS). This prom pted us to analyse activity of antioxidant enzymes in A. pom pejana tissues and investigate w hether they are adjusted to the endogenous production of ROS by oxidative phosphorylations and/or to the environm ental conditions. This was investigated by com paring antioxidant and m etabolic enzyme activities in gills, head, body wall, pygidium and guts of A. pom pejana col lected at different vent sites of the East Pacific Rise. The antioxidant defence arsenal of A. p o m p e jana is peculiar, showing very low catalase (CAT) activity and very high superoxide dism utase (SOD) activity in most tissues. It is very likely that CAT is not expressed in A. pom pejana, as this haem ic enzyme could be inhibited by the high sulphide concentrations prevailing in the worm's environm ent. A. pom pejana does not com pensate 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 m etabolism represents the m ain source of peroxides m anaged 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 anim al's gills and gut, possibly reflecting differences in the vent fluid therm al regim e and/or chemistry.

7.7.4 Alvinellidae Desbruyères & Laubier, 1986

“…Tubes represent a very efficient mean to insulate the worm from high temperatures (Gaill and Bouligand 1987) and from the chaotic variations of temperature over short time intervals (<1 min). Alvinellidae are well-adapted to live in severe hypoxic conditions (see the respiration section) and have high activities of anaerobic and oxidative stress enzymes (Dilly et al 2012, Genard et al 2013). These activities are even more pronounced for species that live in colder but diffuse venting conditions, where H2S concentrations can be higher than on the chimney walls (Rinke and Lee 2009).…”

Adaptation and evolution of the sea anemone Alvinactis sp. to deep‐sea hydrothermal vents: A comparison using transcriptomes

“…Heavy metals can be sequestrated by metallothionein, phytochelatin, or ferritin to avoid their toxicity (Chen et al, 2015;Wong et al, 2015;Zapata et al, 2009). The in vivo effect of metals (like reactive oxygen species [ROS]) causes these organisms to respond by the function of detoxification of superoxide dismutase (SOD), catalase, or glutathione peroxidase (Genard et al, 2013;Marie et al, 2006). Some molecular mechanisms for adaptation to vent environments have also been elucidated.…”

Sensing deep extreme environments: the receptor cell types, brain centers, and multi-layer neural packaging of hydrothermal vent endemic worms

“…The fauna inhabiting these hot spring fields are exposed to highly fluctuating physico-chemical conditions, high levels of heavy metals, sulfide, and carbon dioxide, and harmful compounds such as hydrogen peroxide and hydroxyl radicals [ 3 , 4 ]. The emblematic characteristic of these alvinellids is thus their exceptional tolerance to high temperatures and the toxicity of acidic and reducing fluids [ 5 - 8 ]. Indeed, the alvinellid thermostabilization, detoxification, and anti-oxidative stress capacities have been attributed to a number of biochemical, physiological, and structural properties [ 4 , 9 - 13 ], supported by deep sequencing analysis of the transcriptomic and proteomic level stability [ 14 - 16 ].…”