Effects of intermittent hypoxia on oxidative stress and protein degradation in molluscan mitochondria

J Exp Biol. 2016 Dec 1;219(Pt 23):3794-3802. doi: 10.1242/jeb.146209. Epub 2016 Sep 21.

Abstract

Oxygen fluctuations represent a common stressor in estuarine and intertidal environments and can compromise the mitochondrial integrity and function in marine organisms. We assessed the role of mitochondrial protection mechanisms (ATP-dependent and -independent mitochondrial proteases, and antioxidants) in tolerance to intermittent hypoxia or anoxia in three species of marine bivalves: hypoxia-tolerant hard clams (Mercenaria mercenaria) and oysters (Crassostrea virginica), and a hypoxia-sensitive subtidal scallop (Argopecten irradians). In clams and oysters, mitochondrial tolerance to hypoxia (18 h at 5% O2), anoxia (18 h at 0.1% O2) and subsequent reoxygenation was associated with the ability to maintain the steady-state activity of ATP-dependent and -independent mitochondrial proteases and an anticipatory upregulation of the total antioxidant capacity under the low oxygen conditions. No accumulation of end-products of lipid or protein peroxidation was found during intermittent hypoxia or anoxia in clams and oysters (except for an increase in protein carbonyl concentration after hypoxia-reoxygenation in oysters). In contrast, hypoxia/anoxia and reoxygenation strongly suppressed activity of the ATP-dependent mitochondrial proteases in hypoxia-sensitive scallops. This suppression was associated with accumulation of oxidatively damaged mitochondrial proteins (including carbonylated proteins and proteins conjugated with a lipid peroxidation product malondialdehyde) despite high total antioxidant capacity levels in scallop mitochondria. These findings highlight a key role of mitochondrial proteases in protection against hypoxia-reoxygenation stress and adaptations to frequent oxygen fluctuations in intertidal mollusks.

Keywords: ATP-dependent proteases; Antioxidants; Bivalves; Hypoxia–reoxygenation; Mitoproteases; Oxidative lesions.

MeSH terms

  • Animals
  • Antioxidants / metabolism
  • Cell Hypoxia / physiology*
  • Crassostrea / metabolism*
  • Mercenaria / metabolism*
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / metabolism
  • Oxidative Stress / physiology*
  • Oxygen / metabolism
  • Pectinidae / metabolism*
  • Peptide Hydrolases / metabolism
  • Proteolysis*

Substances

  • Antioxidants
  • Mitochondrial Proteins
  • Peptide Hydrolases
  • Oxygen