Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis

Hypoxia is common in marine environments and a major stressor for marine organisms inhabiting benthic and intertidal zones. Several studies have explored the responses of these organisms to hypoxic stress at the whole organism level with a focus on energy metabolism and mitochondrial response, but t...

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Autores principales: Eugene P. Sokolov, Linda Adzigbli, Stephanie Markert, Amanda Bundgaard, Angela Fago, Dörte Becher, Claudia Hirschfeld, Inna M. Sokolova
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:833ae66eacfc4998bd005a97becdceac2021-11-05T05:46:51ZIntrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis2296-774510.3389/fmars.2021.773734https://doaj.org/article/833ae66eacfc4998bd005a97becdceac2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmars.2021.773734/fullhttps://doaj.org/toc/2296-7745Hypoxia is common in marine environments and a major stressor for marine organisms inhabiting benthic and intertidal zones. Several studies have explored the responses of these organisms to hypoxic stress at the whole organism level with a focus on energy metabolism and mitochondrial response, but the instrinsic mitochondrial responses that support the organelle’s function under hypoxia and reoxygenation (H/R) stress are not well understood. We studied the effects of acute H/R stress (10 min anoxia followed by 15 min reoxygenation) on mitochondrial respiration, production of reactive oxygen species (ROS) and posttranslational modifications (PTM) of the proteome in a marine facultative anaerobe, the blue mussel Mytilus edulis. The mussels’ mitochondria showed increased OXPHOS respiration and suppressed proton leak resulting in a higher coupling efficiency after H/R stress. ROS production decreased in both the resting (LEAK) and phosphorylating (OXPHOS) state indicating that M. edulis was able to prevent oxidative stress and mitochondrial damage during reoxygenation. Hypoxia did not lead to rearrangement of the mitochondrial supercomplexes but impacted the mitochondrial phosphoproteome including the proteins involved in OXPHOS, amino acid- and fatty acid catabolism, and protein quality control. This study indicates that mussels’ mitochondria possess intrinsic mechanisms (including regulation via reversible protein phosphorylation) that ensure high respiratory flux and mitigate oxidative damage during H/R stress and contribute to the hypoxia-tolerant mitochondrial phenotype of this metabolically plastic species.Eugene P. SokolovLinda AdzigbliLinda AdzigbliStephanie MarkertStephanie MarkertAmanda BundgaardAngela FagoDörte BecherClaudia HirschfeldInna M. SokolovaInna M. SokolovaFrontiers Media S.A.articlebioenergeticsmitochondriarespirationoxidative stressproteomicsposttranslational modification (PTM)ScienceQGeneral. Including nature conservation, geographical distributionQH1-199.5ENFrontiers in Marine Science, Vol 8 (2021)
institution DOAJ
collection DOAJ
language EN
topic bioenergetics
mitochondria
respiration
oxidative stress
proteomics
posttranslational modification (PTM)
Science
Q
General. Including nature conservation, geographical distribution
QH1-199.5
spellingShingle bioenergetics
mitochondria
respiration
oxidative stress
proteomics
posttranslational modification (PTM)
Science
Q
General. Including nature conservation, geographical distribution
QH1-199.5
Eugene P. Sokolov
Linda Adzigbli
Linda Adzigbli
Stephanie Markert
Stephanie Markert
Amanda Bundgaard
Angela Fago
Dörte Becher
Claudia Hirschfeld
Inna M. Sokolova
Inna M. Sokolova
Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis
description Hypoxia is common in marine environments and a major stressor for marine organisms inhabiting benthic and intertidal zones. Several studies have explored the responses of these organisms to hypoxic stress at the whole organism level with a focus on energy metabolism and mitochondrial response, but the instrinsic mitochondrial responses that support the organelle’s function under hypoxia and reoxygenation (H/R) stress are not well understood. We studied the effects of acute H/R stress (10 min anoxia followed by 15 min reoxygenation) on mitochondrial respiration, production of reactive oxygen species (ROS) and posttranslational modifications (PTM) of the proteome in a marine facultative anaerobe, the blue mussel Mytilus edulis. The mussels’ mitochondria showed increased OXPHOS respiration and suppressed proton leak resulting in a higher coupling efficiency after H/R stress. ROS production decreased in both the resting (LEAK) and phosphorylating (OXPHOS) state indicating that M. edulis was able to prevent oxidative stress and mitochondrial damage during reoxygenation. Hypoxia did not lead to rearrangement of the mitochondrial supercomplexes but impacted the mitochondrial phosphoproteome including the proteins involved in OXPHOS, amino acid- and fatty acid catabolism, and protein quality control. This study indicates that mussels’ mitochondria possess intrinsic mechanisms (including regulation via reversible protein phosphorylation) that ensure high respiratory flux and mitigate oxidative damage during H/R stress and contribute to the hypoxia-tolerant mitochondrial phenotype of this metabolically plastic species.
format article
author Eugene P. Sokolov
Linda Adzigbli
Linda Adzigbli
Stephanie Markert
Stephanie Markert
Amanda Bundgaard
Angela Fago
Dörte Becher
Claudia Hirschfeld
Inna M. Sokolova
Inna M. Sokolova
author_facet Eugene P. Sokolov
Linda Adzigbli
Linda Adzigbli
Stephanie Markert
Stephanie Markert
Amanda Bundgaard
Angela Fago
Dörte Becher
Claudia Hirschfeld
Inna M. Sokolova
Inna M. Sokolova
author_sort Eugene P. Sokolov
title Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis
title_short Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis
title_full Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis
title_fullStr Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis
title_full_unstemmed Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis
title_sort intrinsic mechanisms underlying hypoxia-tolerant mitochondrial phenotype during hypoxia-reoxygenation stress in a marine facultative anaerobe, the blue mussel mytilus edulis
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/833ae66eacfc4998bd005a97becdceac
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