Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas

Coastal environments commonly experience fluctuations in salinity and hypoxia–reoxygenation (H/R) stress that can negatively affect mitochondrial functions of marine organisms. Although intertidal bivalves are adapted to these conditions, the mechanisms that sustain mitochondrial integrity and funct...

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Published in:Journal of Experimental Biology
Main Authors: Steffen, Jennifer B. M., Sokolov, Eugene P., Bock, Christian, Sokolova, Inna M.
Format: Text
Language:English
Published: The Company of Biologists Ltd 2023
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10445735/
http://www.ncbi.nlm.nih.gov/pubmed/37470191
https://doi.org/10.1242/jeb.246164
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spelling ftpubmed:oai:pubmedcentral.nih.gov:10445735 2023-09-26T15:17:24+02:00 Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas Steffen, Jennifer B. M. Sokolov, Eugene P. Bock, Christian Sokolova, Inna M. 2023-08-03 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10445735/ http://www.ncbi.nlm.nih.gov/pubmed/37470191 https://doi.org/10.1242/jeb.246164 en eng The Company of Biologists Ltd http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10445735/ http://www.ncbi.nlm.nih.gov/pubmed/37470191 http://dx.doi.org/10.1242/jeb.246164 © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. J Exp Biol Research Article Text 2023 ftpubmed https://doi.org/10.1242/jeb.246164 2023-08-27T01:12:20Z Coastal environments commonly experience fluctuations in salinity and hypoxia–reoxygenation (H/R) stress that can negatively affect mitochondrial functions of marine organisms. Although intertidal bivalves are adapted to these conditions, the mechanisms that sustain mitochondrial integrity and function are not well understood. We determined the rates of respiration and reactive oxygen species (ROS) efflux in the mitochondria of oysters, Crassostrea gigas, acclimated to high (33 psu) or low (15 psu) salinity, and exposed to either normoxic conditions (control; 21% O(2)) or short-term hypoxia (24 h at <0.01% O(2)) and subsequent reoxygenation (1.5 h at 21% O(2)). Further, we exposed isolated mitochondria to anoxia in vitro to assess their ability to recover from acute (∼10 min) oxygen deficiency (<0.01% O(2)). Our results showed that mitochondria of oysters acclimated to high or low salinity did not show severe damage and dysfunction during H/R stress, consistent with the hypoxia tolerance of C. gigas. However, acclimation to low salinity led to improved mitochondrial performance and plasticity, indicating that 15 psu might be closer to the metabolic optimum of C. gigas than 33 psu. Thus, acclimation to low salinity increased mitochondrial oxidative phosphorylation rate and coupling efficiency and stimulated mitochondrial respiration after acute H/R stress. However, elevated ROS efflux in the mitochondria of low-salinity-acclimated oysters after acute H/R stress indicates a possible trade-off of higher respiration. The high plasticity and stress tolerance of C. gigas mitochondria may contribute to the success of this invasive species and facilitate its further expansion into brackish regions such as the Baltic Sea. Text Crassostrea gigas Pacific oyster PubMed Central (PMC) Pacific Journal of Experimental Biology 226 15
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Article
spellingShingle Research Article
Steffen, Jennifer B. M.
Sokolov, Eugene P.
Bock, Christian
Sokolova, Inna M.
Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas
topic_facet Research Article
description Coastal environments commonly experience fluctuations in salinity and hypoxia–reoxygenation (H/R) stress that can negatively affect mitochondrial functions of marine organisms. Although intertidal bivalves are adapted to these conditions, the mechanisms that sustain mitochondrial integrity and function are not well understood. We determined the rates of respiration and reactive oxygen species (ROS) efflux in the mitochondria of oysters, Crassostrea gigas, acclimated to high (33 psu) or low (15 psu) salinity, and exposed to either normoxic conditions (control; 21% O(2)) or short-term hypoxia (24 h at <0.01% O(2)) and subsequent reoxygenation (1.5 h at 21% O(2)). Further, we exposed isolated mitochondria to anoxia in vitro to assess their ability to recover from acute (∼10 min) oxygen deficiency (<0.01% O(2)). Our results showed that mitochondria of oysters acclimated to high or low salinity did not show severe damage and dysfunction during H/R stress, consistent with the hypoxia tolerance of C. gigas. However, acclimation to low salinity led to improved mitochondrial performance and plasticity, indicating that 15 psu might be closer to the metabolic optimum of C. gigas than 33 psu. Thus, acclimation to low salinity increased mitochondrial oxidative phosphorylation rate and coupling efficiency and stimulated mitochondrial respiration after acute H/R stress. However, elevated ROS efflux in the mitochondria of low-salinity-acclimated oysters after acute H/R stress indicates a possible trade-off of higher respiration. The high plasticity and stress tolerance of C. gigas mitochondria may contribute to the success of this invasive species and facilitate its further expansion into brackish regions such as the Baltic Sea.
format Text
author Steffen, Jennifer B. M.
Sokolov, Eugene P.
Bock, Christian
Sokolova, Inna M.
author_facet Steffen, Jennifer B. M.
Sokolov, Eugene P.
Bock, Christian
Sokolova, Inna M.
author_sort Steffen, Jennifer B. M.
title Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas
title_short Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas
title_full Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas
title_fullStr Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas
title_full_unstemmed Combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the Pacific oyster, Crassostrea gigas
title_sort combined effects of salinity and intermittent hypoxia on mitochondrial capacity and reactive oxygen species efflux in the pacific oyster, crassostrea gigas
publisher The Company of Biologists Ltd
publishDate 2023
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10445735/
http://www.ncbi.nlm.nih.gov/pubmed/37470191
https://doi.org/10.1242/jeb.246164
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source J Exp Biol
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10445735/
http://www.ncbi.nlm.nih.gov/pubmed/37470191
http://dx.doi.org/10.1242/jeb.246164
op_rights © 2023. Published by The Company of Biologists Ltd
https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
op_doi https://doi.org/10.1242/jeb.246164
container_title Journal of Experimental Biology
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