Variations in oxidative stress and antioxidant defense level during different phases of hibernation in common Asian toad,Duttaphrynus melanostictus

Abstract

To assess redox status during hibernation with metabolic depression, oxidative stress parameters and antioxidant defense were assessed during different phases of hibernation including active period, hibernation, arousal, and post arousal period, in the liver and brain tissues of Duttaphrynus melanostictus. We hypothesized low levels of oxidative stress and antioxidant defense during the hibernation period in comparison to the summer active period due to hypometabolism and their subsequent increase during the arousal period following an increase in body temperature and metabolism. Contrary to our hypothesis increased oxidative stress with significantly higher lipid peroxidation, protein carbonylation, GSSG/GSH ratio, and elevated antioxidants defense consisting of higher catalase activity and high ascorbic acid content to control oxidative stress were found during hibernation. However, GSH and uric acid levels were found low with SOD activities at a steady level during hibernation. Supporting our hypothesis increased oxidative stress with high lipid peroxidation and GSSG/GSH ratio were found during arousal from hibernation owing to increased oxygen consumption and rewarming. Augmented catalase and SOD activities and nonenzymatic antioxidants (GSH, ascorbic acid, and uric acid) level were found to counteract oxidative stress during arousal periods as it was expected. A steady level of protein carbonylation indicating no oxidative damage during arousal from hibernation due to elevated antioxidant defense shows the significance of hibernation to overcome food and water scarcity and cold climatic condition. Decrease in antioxidants levels accompanying coming down of lipid peroxidation, protein carbonylation, and GSSG/GSH ratio to their lower levels during post arousal period showing normalcy in redox status as it was during active period indicates controllability of oxidative stress in hibernating toads.

Metabolic and Redox Biomarkers in Skeletal Muscle Underlie Physiological Adaptations of Two Estivating Anuran Species in a South American Semi-arid Environment

“…In the case of Astyanax elachylepis , fish collected in a naturally hypoxic intermittent stream suffer more oxidative damage and have increased GPX activity in gills compared with fish living in a naturally normoxic perennial stream during the dry season ( Ondei et al, 2020 ). More recently, the levels of redox metabolism biomarkers in naturally hibernating common Asian toads, Duttaphrynus melanostictus , at the end of the winter were compared with those in naturally active toads collected during summer ( Patnaik and Sahoo, 2021 ). The redox balance in the brain and liver of hibernating toads shifts toward a more oxidized state (i.e., increased GSSG/GSH ratio; Patnaik and Sahoo, 2021 ).…”

“…More recently, the levels of redox metabolism biomarkers in naturally hibernating common Asian toads, Duttaphrynus melanostictus , at the end of the winter were compared with those in naturally active toads collected during summer ( Patnaik and Sahoo, 2021 ). The redox balance in the brain and liver of hibernating toads shifts toward a more oxidized state (i.e., increased GSSG/GSH ratio; Patnaik and Sahoo, 2021 ). Such a disruption of the redox balance is associated with increased damage to proteins and lipids and the induction of catalase activity in both tissues of hibernating toads compared with active toads ( Patnaik and Sahoo, 2021 ).…”

“…The redox balance in the brain and liver of hibernating toads shifts toward a more oxidized state (i.e., increased GSSG/GSH ratio; Patnaik and Sahoo, 2021 ). Such a disruption of the redox balance is associated with increased damage to proteins and lipids and the induction of catalase activity in both tissues of hibernating toads compared with active toads ( Patnaik and Sahoo, 2021 ). Therefore, evidence from field-collected mussels, fish and anurans, including our previous ( Moreira et al, 2020 ) and present study, indicates the occurrence of POS under ecologically relevant settings.…”

“…Given the large number of studies on the modulation of antioxidants conducted with animals under artificially controlled settings, we have previously set the challenge of assessing POS under natural conditions ( Moreira et al, 2017 ). This challenge was met by few recent studies ( Ondei et al, 2020 ; Moreira et al, 2021 ; Patnaik and Sahoo, 2021 ), including one that evaluated the modulation of endogenous antioxidants in the muscle of Proceratophrys cristiceps (Anura: Odontophrynidae) from the Brazilian Caatinga ( Moreira et al, 2020 ). In addition to the scarcity of studies under field conditions, it is still not known if POS can be generalized to other anuran species estivating in semi-arid environments.…”

The role of solar radiation and tidal emersion on oxidative stress and glutathione synthesis in mussels exposed to air

“…Since almost all POS-related studies, until 2016, were performed in the lab, we proposed a challenge to show more evidence of POS phenotype in animals under natural conditions, i.e., in the wilderness ( Moreira et al, 2017b ). Several studies met this challenge, including the investigation of fish endurance in a seasonal hypoxic stream ( Ondei et al, 2020 ), frog estivation in a semi-desertic region (two species; Moreira et al, 2020 ; Moreira et al, 2021a , toad hibernation in cold mountains in India ( Patnaik & Sahoo, 2021 ), and aerial exposure of mollusks Brachidontes solisianus and Littorina kurila during the low tide ( Istomina, Belcheva & Chelomin, 2013 ; Moreira et al, 2021b ). We also recently highlighted that ultraviolet radiation (UVR) could trigger a POS-response in several invertebrate species with a molecular mechanism similar to hypoxia-induced POS ( Geihs et al, 2020 ).…”