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

Abstract

The upregulation of endogenous antioxidants (i.e., preparation for oxidative stress, POS) is part of the biochemical responses underlying the adaptation of animals to adverse environments. Despite the phylogenetic diversity of animals in which POS has been described, most studies focus on animals under controlled laboratory conditions. To address this limitation, we have recently assessed the redox metabolism in the skeletal muscle of Proceratophrys cristiceps estivating under natural settings in the Caatinga. Here, we analyzed biochemical biomarkers in the muscle of another Caatinga species, Pleurodema diplolister, during the rainy (active) and dry (estivating frogs) seasons. We aimed to determine whether P. diplolister enhances its antioxidants during estivation under field conditions and to identify any effect of species on the biochemical responses of P. diplolister and P. cristiceps associated with estivation. To do so, we measured the activities of representative enzymes of intermediary metabolism and antioxidant systems, as well as glutathione and protein carbonyl levels, in the skeletal muscle of P. diplolister. Our findings revealed the suppression of oxidative metabolism and activation of antioxidant enzymes in estivating P. diplolister compared with active specimens. No changes in oxidative damage to proteins were observed and estivating P. diplolister had lower levels of disulfide glutathione (GSSG) and disulfide-to-total glutathione ratio (GSSG/tGSH) than those observed in active individuals. When data for P. diplolister and P. cristiceps were assembled and analyzed, significant effects of species were detected on the activities of metabolic enzymes (citrate synthase, isocitric dehydrogenase, malic enzyme, and creatine kinase) and antioxidant enzymes (catalase, glutathione peroxidase and glutathione transferase), as well as on GSSG/tGSH ratio. Such effects might underlie the physiological and behavioral differences between these two species that share the same microhabitat and survival strategy (i.e., to estivate) during the dry season. Despite some peculiarities, which reflect the physiological diversity of the mechanisms associated with estivation in the Brazilian Caatinga, both P. diplolister and P. cristiceps seem to balance the suppression of oxidative pathways, the maintenance of the capacity of oxygen-independent pathways, and the activation of endogenous antioxidants to preserve muscle function and be ready to resume activity whenever the unpredictable rainy period arrives.

Metabolic Adaption of Flexor Carpi Radialis to Amplexus Behavior in Asiatic Toads (Bufo gargarizans)

“…The disruption of metabolism in Xenopus has been linked to a decrease in adult recruitment and reproductive success, ultimately affecting the development and fecundity of their offspring [ 27 , 28 ]. Therefore, amphibians need to maintain metabolic homeostasis to adapt to relatively harsh environments (low temperatures, drought, insufficient food, and so on) by regulating their metabolic processes [ 29 , 30 , 31 ]. For instance, amino acids and derivatives and carbohydrates are reduced in Tibetan frogs during winter, suggesting a lower metabolic rate and energy consumption due to winter stress [ 32 ].…”

Glutathione Depletion Disrupts Redox Homeostasis in an Anoxia-Tolerant Invertebrate

“…The upregulation of antioxidant systems under environmental stress was coined “Preparation for Oxidative Stress” (POS) [ 2 , 4 , 5 ], which has been described to occur in over 80 animal species from 8 phyla, under laboratory simulations of harsh environmental conditions [ 6 , 7 ]. More recently, the POS phenotype has also been observed to happen naturally in the field for a few animal taxa, including mollusks [ 8 , 9 , 10 , 11 ].…”

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

“…This kind of biochemical adaptation was originally called ‘preparation for oxidative stress’ (POS) and proposed to be a mechanism that allows animals to deal with the extremes of the environment, especially conditions leading to metabolic depression and/or low oxygen availability ( Giraud-Billoud et al, 2019 ; Moreira et al, 2023 ; Rodriguez, Campoy-Diaz & Giraud-Billoud, 2023 ). The POS mechanism was reported to work in more than 80 animal species when exposed to freezing, hypoxia or anoxia, severe dehydration, and air (water breathing animals), as well as during estivation ( Moreira et al, 2021a ). In addition, the POS phenotype was also documented for eight animal phyla, indicating its broad relevance in the animal kingdom ( Moreira et al, 2017b ).…”

“…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 ).…”