Salinity stress from the perspective of the energy-redox axis: Lessons from a marine intertidal flatworm.
In the context of global change, there is an urgent need for researchers in conservation physiology to understand the physiological mechanisms leading to the acquisition of stress acclimation phenotypes. Intertidal organisms continuously cope with drastic changes in their environmental conditions, making them outstanding models for the study of physiological acclimation. As the implementation of such processes usually comes at a high bioenergetic cost, a mitochondrial/oxidative stress approach emerges as the most relevant approach when seeking to analyze whole-animal responses. Here we use the intertidal flatworm Macrostomum lignano to analyze the bioenergetics of salinity acclimation and its consequences in terms of reactive oxygen/nitrogen species formation and physiological response to counteract redox imbalance. Measures of water fluxes and body volume suggest that M. lignano is a hyper-/iso-regulator. Higher salinities were revealed to be the most energetically expensive conditions, with an increase in mitochondrial density accompanied by increased respiration rates. Such modifications came at the price of enhanced superoxide anion production, likely associated with a high caspase 3 upregulation. These animals nevertheless managed to live at high levels of environmental salinity through the upregulation of several mitochondrial antioxidant enzymes such as superoxide dismutase. Contrarily, animals at low salinities decreased their respiration rates, reduced their activity and increased nitric oxide formation, suggesting a certain degree of metabolic arrest. A contradictory increase in dichlorofluorescein fluorescence and an upregulation of gluthathione-S-transferase pi 1 (GSTP1) expression were observed in these individuals. If animals at low salinity are indeed facing metabolic depression, the return to seawater may result in an oxidative burst. We hypothesize that this increase in GSTP1 could be a "preparation for oxidative stress", i.e. a mechanism to counteract the production of free radicals upon returning to seawater. The results of the present study shed new light on how tolerant organisms carry out subcellular adaptations to withstand environmental change.
Groupe fonctionnel AEO (Adaptation Ecophysiologique et Ontogenèse), UMR 9190 MARBEC, University of Montpellier, 34095 Montpellier, France. Electronic address: georgina.rivera-ingraham@umontpellier.fr.
Georgina A
GA
Rivera-Ingraham
Groupe fonctionnel AEO (Adaptation Ecophysiologique et Ontogenèse), UMR 9190 MARBEC, University of Montpellier, 34095 Montpellier, France.
Aude
A
Nommick
Groupe fonctionnel AEO (Adaptation Ecophysiologique et Ontogenèse), UMR 9190 MARBEC, University of Montpellier, 34095 Montpellier, France.
Eva
E
Blondeau-Bidet
Institute of Zoology and Center for Molecular Biosciences Innsbruck, University of Innsbruck, A-6020 Innsbruck, Austria.
Peter
P
Ladurner
Groupe fonctionnel AEO (Adaptation Ecophysiologique et Ontogenèse), UMR 9190 MARBEC, University of Montpellier, 34095 Montpellier, France.
Jehan-Hervé
JH
Lignot
D000222:Adaptation, Physiological; D000818:Animals; D053148:Caspase 3 / Q000378:metabolism; D004734:Energy Metabolism; D051549:Glutathione S-Transferase pi; D008928:Mitochondria / Q000378:metabolism; D010084:Oxidation-Reduction; D010986:Platyhelminths / Q000254:growth & development* / Q000378:metabolism; D026361:Reactive Nitrogen Species / Q000378:metabolism*; D017382:Reactive Oxygen Species / Q000378:metabolism*; D054712:Salinity; D013312:Stress, Physiological; D015854:Up-Regulation
D026361:Reactive Nitrogen Species; D017382:Reactive Oxygen Species; D051549:Glutathione S-Transferase pi; D053148:Caspase 3
Energetic balance; Flatworms; Live-imaging; Mitochondrial membrane potential; Osmoregulation; RNS; ROS
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