Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica
Oxygen fluctuations are common in marine waters, and hypoxia– reoxygenation (H–R) stress can negatively affect mitochondrial metabolism. The long-lived ocean quahog, Arctica islandica, is known for its hypoxia tolerance associated with metabolic rate depression, yet the mechanisms that sustain mitoc...
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ftawi:oai:epic.awi.de:55348 2024-09-15T17:54:28+00:00 Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica Steffen, Jennifer B. M. Haider, Fouzia Sokolov, Eugene P. Bock, Christian Sokolova, Inna M. 2021-10-06 application/pdf https://epic.awi.de/id/eprint/55348/ https://epic.awi.de/id/eprint/55348/1/JSteffen_mito_cap_JEB21.pdf https://doi.org/10.1242/jeb.243082 https://hdl.handle.net/10013/epic.ab321016-d845-4c35-9f13-df065062c857 unknown https://epic.awi.de/id/eprint/55348/1/JSteffen_mito_cap_JEB21.pdf Steffen, J. B. M. , Haider, F. , Sokolov, E. P. , Bock, C. orcid:0000-0003-0052-3090 and Sokolova, I. M. (2021) Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica , Journal of Experimental Biology, 224 (21) . doi:10.1242/jeb.243082 <https://doi.org/10.1242/jeb.243082> , hdl:10013/epic.ab321016-d845-4c35-9f13-df065062c857 EPIC3Journal of Experimental Biology, 224(21), ISSN: 0022-0949 Article isiRev 2021 ftawi https://doi.org/10.1242/jeb.243082 2024-06-24T04:27:29Z Oxygen fluctuations are common in marine waters, and hypoxia– reoxygenation (H–R) stress can negatively affect mitochondrial metabolism. The long-lived ocean quahog, Arctica islandica, is known for its hypoxia tolerance associated with metabolic rate depression, yet the mechanisms that sustain mitochondrial function during oxygen fluctuations are not well understood. We used top-down metabolic control analysis (MCA) to determine aerobic capacity and control over oxygen flux in the mitochondria of quahogs exposed to short-term hypoxia (24 h <0.01% O2) and subsequent reoxygenation (1.5 h 21% O2) compared with normoxic control animals (21% O2). We demonstrated that flux capacity of the substrate oxidation and proton leak subsystems were not affected by hypoxia, while the capacity of the phosphorylation subsystem was enhanced during hypoxia associated with a depolarization of the mitochondrial membrane. Reoxygenation decreased the oxygen flux capacity of all three mitochondrial subsystems. Control over oxidative phosphorylation (OXPHOS) respiration was mostly exerted by substrate oxidation regardless of H–R stress, whereas control by the proton leak subsystem of LEAK respiration increased during hypoxia and returned to normoxic levels during reoxygenation. During hypoxia, reactive oxygen species (ROS) efflux was elevated in the LEAK state, whereas it was suppressed in the OXPHOS state. Mitochondrial ROS efflux returned to normoxic control levels during reoxygenation. Thus, mitochondria of A. islandica appear robust to hypoxia by maintaining stable substrate oxidation and upregulating phosphorylation capacity, but remain sensitive to reoxygenation. This mitochondrial phenotype might reflect adaptation of A. islandica to environments with unpredictable oxygen fluctuations and its behavioural preference for low oxygen levels. Article in Journal/Newspaper Arctica islandica Ocean quahog Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center) Journal of Experimental Biology 224 21 |
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Open Polar |
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Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center) |
op_collection_id |
ftawi |
language |
unknown |
description |
Oxygen fluctuations are common in marine waters, and hypoxia– reoxygenation (H–R) stress can negatively affect mitochondrial metabolism. The long-lived ocean quahog, Arctica islandica, is known for its hypoxia tolerance associated with metabolic rate depression, yet the mechanisms that sustain mitochondrial function during oxygen fluctuations are not well understood. We used top-down metabolic control analysis (MCA) to determine aerobic capacity and control over oxygen flux in the mitochondria of quahogs exposed to short-term hypoxia (24 h <0.01% O2) and subsequent reoxygenation (1.5 h 21% O2) compared with normoxic control animals (21% O2). We demonstrated that flux capacity of the substrate oxidation and proton leak subsystems were not affected by hypoxia, while the capacity of the phosphorylation subsystem was enhanced during hypoxia associated with a depolarization of the mitochondrial membrane. Reoxygenation decreased the oxygen flux capacity of all three mitochondrial subsystems. Control over oxidative phosphorylation (OXPHOS) respiration was mostly exerted by substrate oxidation regardless of H–R stress, whereas control by the proton leak subsystem of LEAK respiration increased during hypoxia and returned to normoxic levels during reoxygenation. During hypoxia, reactive oxygen species (ROS) efflux was elevated in the LEAK state, whereas it was suppressed in the OXPHOS state. Mitochondrial ROS efflux returned to normoxic control levels during reoxygenation. Thus, mitochondria of A. islandica appear robust to hypoxia by maintaining stable substrate oxidation and upregulating phosphorylation capacity, but remain sensitive to reoxygenation. This mitochondrial phenotype might reflect adaptation of A. islandica to environments with unpredictable oxygen fluctuations and its behavioural preference for low oxygen levels. |
format |
Article in Journal/Newspaper |
author |
Steffen, Jennifer B. M. Haider, Fouzia Sokolov, Eugene P. Bock, Christian Sokolova, Inna M. |
spellingShingle |
Steffen, Jennifer B. M. Haider, Fouzia Sokolov, Eugene P. Bock, Christian Sokolova, Inna M. Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica |
author_facet |
Steffen, Jennifer B. M. Haider, Fouzia Sokolov, Eugene P. Bock, Christian Sokolova, Inna M. |
author_sort |
Steffen, Jennifer B. M. |
title |
Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica |
title_short |
Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica |
title_full |
Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica |
title_fullStr |
Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica |
title_full_unstemmed |
Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica |
title_sort |
mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, arctica islandica |
publishDate |
2021 |
url |
https://epic.awi.de/id/eprint/55348/ https://epic.awi.de/id/eprint/55348/1/JSteffen_mito_cap_JEB21.pdf https://doi.org/10.1242/jeb.243082 https://hdl.handle.net/10013/epic.ab321016-d845-4c35-9f13-df065062c857 |
genre |
Arctica islandica Ocean quahog |
genre_facet |
Arctica islandica Ocean quahog |
op_source |
EPIC3Journal of Experimental Biology, 224(21), ISSN: 0022-0949 |
op_relation |
https://epic.awi.de/id/eprint/55348/1/JSteffen_mito_cap_JEB21.pdf Steffen, J. B. M. , Haider, F. , Sokolov, E. P. , Bock, C. orcid:0000-0003-0052-3090 and Sokolova, I. M. (2021) Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica , Journal of Experimental Biology, 224 (21) . doi:10.1242/jeb.243082 <https://doi.org/10.1242/jeb.243082> , hdl:10013/epic.ab321016-d845-4c35-9f13-df065062c857 |
op_doi |
https://doi.org/10.1242/jeb.243082 |
container_title |
Journal of Experimental Biology |
container_volume |
224 |
container_issue |
21 |
_version_ |
1810430788394549248 |