Salinity stress from the perspective of the energy-redox axis: Lessons from a marine intertidal flatworm

Type Article
Date 2016-12
Language English
Author(s) Rivera-Ingraham Georgina A.ORCID1, Nommick Aude1, Blondeau-Bidet EvaORCID1, Ladurner PeterORCID2, 3, Lignot Jehan-Herve1
Affiliation(s) 1 : Univ Montpellier, Grp Fonct AEO Adaptat Ecophysiol & Ontogenese, UMR MARBEC 9190, F-34095 Montpellier, France.
2 : Univ Innsbruck, Inst Zool, A-6020 Innsbruck, Austria.
3 : Univ Innsbruck, Ctr Mol Biosci Innsbruck, A-6020 Innsbruck, Austria.
Source Redox Biology (2213-2317) (Elsevier Science Bv), 2016-12 , Vol. 10 , P. 53-64
DOI 10.1016/j.redox.2016.09.012
WOS© Times Cited 21
Keyword(s) Energetic balance, Flatworms, Live-imaging, Mitochondrial membrane potential, Osmoregulation, RNS, ROS
Abstract

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.

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