Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergetics

Fish in their natural environments possess elaborate mechanisms that regulate physiological function to mitigate the adverse effects of multiple environmental stressors such as temperature, metals, and hypoxia. We investigated how warm acclimation affects mitochondrial responses to Cd, hypoxia, and...

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Main Authors: John O. Onukwufor, Collins Kamunde
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324015264
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author John O. Onukwufor
Collins Kamunde
author_facet John O. Onukwufor
Collins Kamunde
author_sort John O. Onukwufor
collection DOAJ
description Fish in their natural environments possess elaborate mechanisms that regulate physiological function to mitigate the adverse effects of multiple environmental stressors such as temperature, metals, and hypoxia. We investigated how warm acclimation affects mitochondrial responses to Cd, hypoxia, and acute temperature shifts (heat shock and cold snap) in rainbow trout. We observed that state 3 respiration driven by complex I (CI) was resistant to the stressors while warm acclimation and Cd reduced complex I +II (CI + II) driven state 3 respiration. In contrast, state 4 (leak) respirations for both CI and CI + II were consistently stimulated by warm acclimation resulting in reduced mitochondrial coupling efficiency (respiratory control ratio [RCR]). Warm acclimation and Cd exacerbated their individual effect on leak respiration to further reduce the RCR. Moreover, the effect of warm acclimation on mitochondrial bioenergetics aligned with its inhibitory effect on activities of citrate synthase and both CI and CII. Unlike the Cd and warm acclimation combined exposure, hypoxia alone and in combination with warm acclimation and/or Cd abolished the stimulation of CI and CI + II powered leak respirations resulting in partial recovery of RCR. The response to acute temperature shifts indicated that while state 3 respiration returned to pre-acclimation level, the leak respiration did not. Overall, our findings suggest a complex in vivo interaction of multiple stressors on mitochondrial function that are not adequately predicted by their individual effects.
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spelling doaj-art-aabe80fca2ed4748ae95539dd6d290462025-01-23T05:25:36ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01289117450Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergeticsJohn O. Onukwufor0Collins Kamunde1Department of Pharmacology and Physiology, University of Rochester Medical Center, Rochester, NY 14642, USA; Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE C1A 4P3, Canada; Correspondence to: Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE C1A 4P3, Canada.Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE C1A 4P3, Canada; Correspondence to: Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE C1A 4P3, Canada.Fish in their natural environments possess elaborate mechanisms that regulate physiological function to mitigate the adverse effects of multiple environmental stressors such as temperature, metals, and hypoxia. We investigated how warm acclimation affects mitochondrial responses to Cd, hypoxia, and acute temperature shifts (heat shock and cold snap) in rainbow trout. We observed that state 3 respiration driven by complex I (CI) was resistant to the stressors while warm acclimation and Cd reduced complex I +II (CI + II) driven state 3 respiration. In contrast, state 4 (leak) respirations for both CI and CI + II were consistently stimulated by warm acclimation resulting in reduced mitochondrial coupling efficiency (respiratory control ratio [RCR]). Warm acclimation and Cd exacerbated their individual effect on leak respiration to further reduce the RCR. Moreover, the effect of warm acclimation on mitochondrial bioenergetics aligned with its inhibitory effect on activities of citrate synthase and both CI and CII. Unlike the Cd and warm acclimation combined exposure, hypoxia alone and in combination with warm acclimation and/or Cd abolished the stimulation of CI and CI + II powered leak respirations resulting in partial recovery of RCR. The response to acute temperature shifts indicated that while state 3 respiration returned to pre-acclimation level, the leak respiration did not. Overall, our findings suggest a complex in vivo interaction of multiple stressors on mitochondrial function that are not adequately predicted by their individual effects.http://www.sciencedirect.com/science/article/pii/S0147651324015264AcclimationCdHypoxiaPlasticityMitochondrial bioenergeticsRainbow trout
spellingShingle John O. Onukwufor
Collins Kamunde
Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergetics
Ecotoxicology and Environmental Safety
Acclimation
Cd
Hypoxia
Plasticity
Mitochondrial bioenergetics
Rainbow trout
title Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergetics
title_full Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergetics
title_fullStr Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergetics
title_full_unstemmed Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergetics
title_short Interactive effects of temperature, cadmium, and hypoxia on rainbow trout (Oncorhynchus mykiss) liver mitochondrial bioenergetics
title_sort interactive effects of temperature cadmium and hypoxia on rainbow trout oncorhynchus mykiss liver mitochondrial bioenergetics
topic Acclimation
Cd
Hypoxia
Plasticity
Mitochondrial bioenergetics
Rainbow trout
url http://www.sciencedirect.com/science/article/pii/S0147651324015264
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