High anoxia tolerance in the subterranean salamander Proteus anguinus without oxidative stress nor activation of antioxidant defenses during reoxygenation

Abstract

The present study describes a high anoxia tolerance in an amphibian at high temperature. Indeed, the subterranean salamander Proteus anguinus survived 12 h under anoxia at 12 degrees C. Surprisingly, such experimental conditions did not affect P. anguinus oxidative status while muscles and liver antioxidant enzymes activities decreased under 8 h anoxia and only return to basal level during reoxygenation. To test if such adaptation is common in Urodels, equivalent experimentations have been conducted on another newt: the stream-dwelling Calotriton asper. This latter species exhibited only 1.5 h survival under anoxia in spite of higher antioxidant enzymes activities than P. anguinus. Furthermore, aerobic recovery after 1 h anoxia induced a 30% increase of oxidative damage partly explained by SOD and CAT activities that did not return to control values during reoxygenation, demonstrating a lower capacity to counteract ROS overproduction than P. anguinus. In addition, uncoupling protein (UCP) transcript was for the first time detected, partly sequenced and quantified in amphibian muscles and liver. UCP may be considered as a ROS production attenuator by mediating a discharge of the proton gradient generated by the respiratory chain. The putative role of UCP in post-anoxic oxidative status of both species is discussed.

Extreme lifespan of the human fish ( Proteus anguinus ): a challenge for ageing mechanisms

“…It is therefore predicted that species with different longevities also differ in their efficiency of such antioxidant mechanisms [24,25]. However, the olm displays neither remarkable antioxidant activity when compared with other species, nor high cellular damage at an age of 28 years ( [26]; see electronic supplementary material, table S1). In other words, the olm presents a paradox, since neither its basal metabolic rate nor its antioxidant activity, the two most cited mechanisms that should be involved in enhancing lifespan, differ from species with a more reduced lifespan.…”

Preparation for oxidative stress under hypoxia and metabolic depression: Revisiting the proposal two decades later

“…Examples are salamanders under anoxia exposure (Issartel et al, 2009), three fish species under hypoxia (Leveelahti et al, 2014), golden gall fly larvae exposed to freezing (Joanisse and Storey, 1998), and in the fish Heteropneustes fossilis exposed to air exposure (Paital, 2013(Paital, , 2014 Storey, 1996). Moreover, the ratio GSSG:GSH-eq was also increased in muscle after 30 h anoxia and in liver at 10 and 30 h of anoxia, followed by a decrease in the GSSG:GSH-eq ratio during recovery.…”

“…To some extent, our proposal is a simplification of a complex process that may be affected by the action of RNS (section 8), protein chaperones (Storey and Storey, 2011;Trübenbach et al, 2014), uncoupling proteins (UCPs 2 and 3 seen to control mitochondrial ROS formation; Issartel et al, 2009) as well as the presence of nonenzymatic compounds such as ascorbate (Rice et al, 2002) or uric acid (GiraudBilloud et al, 2011).…”

In situUnderwater Tagging of Aquatic Organisms: A Test Using the Cave-Dwelling Olm,Proteus anguinus

“…It is the only member of the family Proteidae and the only obligate cave-dwelling vertebrate in Europe, showing remarkable adaptations to its unique environment. The species is blind, totally depigmented (apart from P. a. parkelj Sket & Arntzen 1994), neotenic, shows high tolerance to anoxia and has long been known for its extreme life-history traits such as its unmatched longevity among anurans (probably over 100 years; only the Japanese giant salamander, Andrias japonica, being comparable) and its resistance to starvation (Hervant et al 2001, Issartel et al 2009, Speakman & Selman 2011, Voituron et al 2011. Despite the long lasting scientific interest, biological knowledge of the species has been gathered mainly from observations and experiments made with captive populations in laboratories.…”