Two faces of one coin: Beneficial and deleterious effects of reactive oxygen species during short-term acclimation to hypo-osmotic stress in a decapod crab

Exposure to environmental changes often results in the production of reactive oxygen species (ROS), which, if uncontrolled, leads to loss of cellular homeostasis and oxidative distress. However, at physiological levels these same ROS are known to be key players in cellular signaling and the regulati...

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Bibliographic Details
Published in:Comparative biochemistry and physiology. Part A, Molecular & integrative physiology Molecular & integrative physiology, 2024-10, Vol.296, p.111700, Article 111700
Main Authors: Rivera-Ingraham, Georgina A., Martínez-Alarcón, Diana, Theuerkauff, Dimitri, Nommick, Aude, Lignot, Jehan-Hervé
Format: Article
Language:English
Subjects:
Crustacean
N-acetyl cysteine
Redox balance
Salinity stress
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Summary:Exposure to environmental changes often results in the production of reactive oxygen species (ROS), which, if uncontrolled, leads to loss of cellular homeostasis and oxidative distress. However, at physiological levels these same ROS are known to be key players in cellular signaling and the regulation of key biological activities (oxidative eustress). While ROS are known to mediate salinity tolerance in plants, little is known for the animal kingdom. In this study, we use the Mediterranean crab Carcinus aestuarii, highly tolerant to salinity changes in its environment, as a model to test the healthy or pathological role of ROS due to exposure to diluted seawater (dSW). Crabs were injected either with an antioxidant [N-acetylcysteine (NAC), 150 mg·kg−1] or phosphate buffered saline (PBS). One hour after the first injection, animals were either maintained in seawater (SW) or transferred to dSW and injections were carried out at 12-h intervals. After ≈48 h of salinity change, all animals were sacrificed and gills dissected for analysis. NAC injections successfully inhibited ROS formation occurring due to dSW transfer. However, this induced 55% crab mortality, as well as an inhibition of the enhanced catalase defenses and mitochondrial biogenesis that occur with decreased salinity. Crab osmoregulatory capacity under dSW condition was not affected by NAC, although it induced in anterior (non-osmoregulatory) gills a 146-fold increase in Na+/K+/2Cl− expression levels, reaching values typically observed in osmoregulatory tissues. We discuss how ROS influences the physiology of anterior and posterior gills, which have two different physiological functions and strategies during hyper-osmoregulation in dSW. [Display omitted] •Antioxidants were used to test the role of free radicals in stress acclimation.•N-acetylcysteine inhibited ROS formation occurring during hypo-osmotic shock.•Quenching ROS inhibits acclimation mechanisms (i.e. increased antioxidant defenses).•Acclimation mechanisms differ between anterior and posterior gills.•The inhibition of ROS formation affects differently anterior and posterior gills.
ISSN:1095-6433
1531-4332
1531-4332
DOI:10.1016/j.cbpa.2024.111700