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

TY - JOUR

T1 - Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis

AU - Sokolov, Eugene P.

AU - Adzigbli, Linda

AU - Markert, Stephanie

AU - Bundgaard, Amanda

AU - Fago, Angela

AU - Becher, Dörte

AU - Hirschfeld, Claudia

AU - Sokolova, Inna M.

PY - 2021/11

Y1 - 2021/11

N2 - 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.

AB - 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.

KW - bioenergetics

KW - bivalve

KW - mitochondria

KW - oxidative stress

KW - posttranslational modification (PTM)

KW - proteomics

KW - respiration

KW - supercomplexes

UR - http://www.scopus.com/inward/record.url?scp=85119402741&partnerID=8YFLogxK

U2 - 10.3389/fmars.2021.773734

DO - 10.3389/fmars.2021.773734

M3 - Journal article

AN - SCOPUS:85119402741

SN - 2296-7745

VL - 8

JO - Frontiers in Marine Science

JF - Frontiers in Marine Science

M1 - 773734

ER -