Redox physiology in animal function: The struggle of living in an oxidant environment (original) (raw)
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How widespread is preparation for oxidative stress in the animal kingdom
It is well known that many anoxia/hypoxia tolerant species when exposed to anoxia/hypoxia respond by increasing the activity/expression of antioxidant enzymes and/or glutathione levels—a phenomenon called " preparation for oxidative stress " (POS). This phenomenon was also observed during freezing exposure, severe dehydration, aerial exposure of water-breathing animals and estivation. However, as far as we know, there is no analysis available of the prevalence of POS among animal species. A major problem is the very definition of POS, since many animal species show both increases and decreases of antioxidants during low oxygen stress and estivation. Therefore, we established three different criteria; from inclusive to restrictive and analyzed how widespread the POS phenomenon is in the animal kingdom. We analyzed all available papers in several databases about the modulation of antioxidant defenses during oxygen deprivation or estivation. Based on the magnitude of change (as % change) during the specific low oxygen stresses or estivation, we classified each species as POS-positive, POS-negative or POS-neutral, considering the three different criteria. The prevalence of POS-positive animals (102 species from 8 phyla) was stress-dependent: in estivation and dehydration it was 91–100%, while in hypoxia it was 37.5–53%, depending on the criteria. In the case of air exposure, anoxia and freezing the proportions of POS-positive species were 54–77%, 64–77% and 75–86%, respectively. Overall, the prevalence of POS was 58 to 68% when all stresses and all species were analyzed together. The results indicate the key importance of POS as a survival strategy of animals exposed to freezing, dehydration and estivation, and, to a lesser extent, to oxygen deprivation itself (i.e. hypoxia and anoxia).
Ecology Letters, 2009
The concept of trade-offs is central to our understanding of life-history evolution. The underlying mechanisms, however, have been little studied. Oxidative stress results from a mismatch between the production of damaging reactive oxygen species (ROS) and the organismÕs capacity to mitigate their damaging effects. Managing oxidative stress is likely to be a major determinant of life histories, as virtually all activities generate ROS. There is a recent burgeoning of interest in how oxidative stress is related to different components of animal performance. The emphasis to date has been on immediate or short-term effects, but there is an increasing realization that oxidative stress will influence life histories over longer time scales. The concept of oxidative stress is currently used somewhat loosely by many ecologists, and the erroneous assumption often made that dietary antioxidants are necessarily the major line of defence against ROS-induced damage. We summarize current knowledge on how oxidative stress occurs and the different methods for measuring it, and highlight where ecologists can be too simplistic in their approach. We critically review the potential role of oxidative stress in mediating life-history trade-offs, and present a framework for formulating appropriate hypotheses and guiding experimental design. We indicate throughout potentially fruitful areas for further research.
Oxidative stress in ecology and evolution: lessons from avian studies
Ecology Letters, 2008
Although oxidative stress is a central topic in biochemical and medical research, the number of reports on its relevance in life-history studies of non-human animals is still low. Information about oxidative stress in wild birds may help describe functional interactions among the components of life-history traits. Currently available evidence suggests that oxidative stress may impart an important physiological cost on longevity, reproduction, immune response or intense physical activity. Given the gaps in our present knowledge, it is still premature to attempt to draw definitive conclusions and basic questions (e.g. how is oxidative stress generated and how do organisms cope with it?) have yet to be fully explored under natural conditions. Therefore, caution is needed in developing hypotheses or drawing general conclusions until additional data become available to perform more rigorous comparative analyses.
The Challenges of Integrating Oxidative Stress into Life-history Biology
BioScience, 2011
It has been proposed that the molecular and physiological systems that regulate biological functions impose costs and constraints that are fundamental to the understanding of variation in life histories. In particular, studies of oxidative stress emphasize how evolutionary contingency can impose novel trade-offs for organisms, and how this may create or eliminate functional linkages between traits. Here, we critically assess the conceptual and empirical basis for these claims and what they mean for the study of life-history variation. Two key challenges are to go beyond the current focus on single components of regulatory systems, assessed at single points in time, and to establish the importance of trait-and stagespecific nutrient requirements for the functional linkage between life-history traits. Furthermore, future progress will critically depend on the replication of laboratory studies in natural settings to target the complexity of trade-off regulation in the wild.
Scientifica, 2016
Antioxidant defence system, a highly conserved biochemical mechanism, protects organisms from harmful effects of reactive oxygen species (ROS), a by-product of metabolism. Both invertebrates and vertebrates are unable to modify environmental physical factors such as photoperiod, temperature, salinity, humidity, oxygen content, and food availability as per their requirement. Therefore, they have evolved mechanisms to modulate their metabolic pathways to cope their physiology with changing environmental challenges for survival. Antioxidant defences are one of such biochemical mechanisms. At low concentration, ROS regulates several physiological processes, whereas at higher concentration they are toxic to organisms because they impair cellular functions by oxidizing biomolecules. Seasonal changes in antioxidant defences make species able to maintain their correct ROS titre to take various physiological functions such as hibernation, aestivation, migration, and reproduction against chan...
Animal response to drastic changes in oxygen availability and physiological oxidative stress
Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 2002
Oxygen is essential for most life forms, but it is also inherently toxic due to its biotransformation into reactive oxygen species (ROS). In fact, the development of many animal and plant pathological conditions, as well as natural aging, is associated with excessive ROS production andyor decreased antioxidant capacity. However, a number of animal species are able to tolerate, under natural conditions, situations posing a large potential for oxidative stress. Situations range from anoxia in fish, frogs and turtles, to severe hypoxia in organs of freeze-tolerant snakes, frogs and insect larvae, or diving seals and turtles, and mild hypoxia in organs of dehydrated frogs and toads or estivating snails. All situations are reminiscent of ischemiayreperfusion events that are highly damaging to most mammals and birds. This article reviews the responses of anoxiayhypoxia-tolerant animals when subjected to environmental and metabolic stresses leading to oxygen limitation. Abrupt changes in metabolic rate in ground squirrels arousing from hibernation, as well as snails arousing from estivation, may also set up a condition of increased ROS formation. Comparing the responses from these diverse animals, certain patterns emerge. The most commonly observed response is an enhancement of the antioxidant defense. The increase in the baseline activity of key antioxidant enzymes, as well as 'secondary' enzymatic defenses, andyor glutathione levels in preparation for a putative oxidative stressful situation arising from tissue reoxygenation seem to be the preferred evolutionary adaptation. Increasing the overall antioxidant capacity during anoxiayhypoxia is of relevance for species such as garter snakes (Thamnophis sirtalis parietalis) and wood fogs (Rana sylvatica), while diving freshwater turtles (Trachemys scripta elegans) appear to rely mainly upon high constitutive activities of antioxidant enzymes to deal with oxidative stress arising during tissue reoxygenation. The possibility that some animal species might control post-anoxic ROS generation cannot be excluded.
Integrative Zoology, 2011
Recent research suggests that oxidative stress, via its links to metabolism and senescence, is a key mechanism linking life history traits such as fecundity and growth with survival; however, this has rarely been put under empirical scrutiny within free-living populations. Using a wild population of live-bearing skinks, we explored how plasma antioxidant activity (OXY), reactive oxidative metabolites (ROM), and the estimated oxidative stress index are associated with female and male life history. We found that male skinks have a significantly higher ROM and estimated oxidative stress index than female skinks, but this was not accompanied by a sex difference in mortality. Both sexes showed a non-linear association between OXY and age, indicating that the oldest and youngest individuals had the lowest OXY. Interestingly, female skinks with high OXY showed a decreased probability of survival to the following season. However, we found no significant associations between female reproductive investment (litter size or litter mass) or parturition date (i.e. metabolism) and oxidative status. Combined, our results offer mixed support for a role of oxidative stress in mediating life history traits and suggest that future studies need to explore oxidative stress during vitellogenesis in addition to using an intra-individual approach to understand the cost of reproduction and patterns of aging.
Oxidative stress decreases with elevation in the lizard Psammodromus algirus
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2014
Oxidative stress is considered one of the main ecological and evolutionary forces. Several environmental stressors vary geographically and thus organisms inhabiting different sites face different oxidant environments. Nevertheless, there is scarce information about how oxidative damage and antioxidant defences vary geographically in animals. Here we study how oxidative stress varies from lowlands (300-700 m asl) to highlands (2200-2500 m asl) in the lizard Psammodromus algirus. To accomplish this, antioxidant enzymatic activity (catalase, superoxide dismutase, glutathione peroxidase, glutathione reductase, glutathione transferase, DT-diaphorase) and lipid peroxidation were assayed in tissue samples from the lizards' tail. Lipid peroxidation was higher in individuals from lowlands than from highlands, indicating higher oxidative stress in lowland lizards. These results suggest that environmental conditions are less oxidant at high elevations with respect to low ones. Therefore, our study shows that oxidative stress varies geographically, which should have important consequences for our understanding of geographic variation in physiology and life-history of organisms.