Differences in heavy metal concentrations and in the response of the antioxidant system to hypoxia and air exposure in the Antarctic limpet Nacella concinna

Abstract

During the austral spring and summer months, the Antarctic limpet Nacella concinna colonizes intertidal environments in the Western Antarctica Peninsula region. The species is divided into a permanently sub-littoral and a seasonally intertidal, migratory subpopulation. We investigate the physiological differentiation between the two limpet groups to identify cellular and molecular changes that accompany adaptation of stenothermal Antarctic invertebrates to life under more stressful intertidal habitat conditions. A major difference between the two groups is the significantly higher concentrations of heavy metals (Fe, Al, Zn) from ingested sediments in sub-littoral limpet digestive glands (DG), associated with higher rates of reactive oxygen species (ROS) formation in this organ. ROS formation is accompanied by significantly higher SOD activity in sub-littoral limpet DG. These high SOD activities are, however, not conserved during either air exposure or hypoxic stress exposure of the sub-littoral limpets, when ROS production is slowed due to the absence of oxygen. The intertidal animals maintain higher levels of SOD and also conserve catalase activity at higher levels during hypoxia or air exposure compared to sub-littoral individuals under the same exposure conditions. More oxidized redox potential in gills and foot muscle and higher antioxidant enzyme activities in gills indicate that intertidal limpets maintain more oxygenated tissues during air exposure, in keeping with shell-lifting for oxygen up-take by the gills of intertidal limpets which migrate up the shore in the spring and down in the autumn. An increase of the redox ratio (GSSG/GSH) and accumulation of the lipid oxidation derived malonedialdehyde in intertidal limpet foot muscle during 12h of exposure to air shows that indeed this tissue becomes more oxidized before the limpets eventually contract their shells tightly to minimize water loss and eventually become anaerobic. Intertidal limpets obviously avoid early onset of anaerobic energy production seen in their sub-littoral congeners when exposed to air and are still able to maintain tissue redox ratio balance when exposed to air.