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Research Article
Rapid mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oyster, Crassostrea gigas
Rossana Sussarellu, Tony Dudognon, Caroline Fabioux, Philippe Soudant, Dario Moraga, Edouard Kraffe
Journal of Experimental Biology 2013 216: 1561-1569; doi: 10.1242/jeb.075879
Rossana Sussarellu
UMR CNRS 6539-LEMAR (Laboratoire des Sciences de l'Environnement Marin), Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale, Technopôle Brest Iroise, 29280 Plouzané, France
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Tony Dudognon
UMR CNRS 6539-LEMAR (Laboratoire des Sciences de l'Environnement Marin), Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale, Technopôle Brest Iroise, 29280 Plouzané, France
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Caroline Fabioux
UMR CNRS 6539-LEMAR (Laboratoire des Sciences de l'Environnement Marin), Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale, Technopôle Brest Iroise, 29280 Plouzané, France
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Philippe Soudant
UMR CNRS 6539-LEMAR (Laboratoire des Sciences de l'Environnement Marin), Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale, Technopôle Brest Iroise, 29280 Plouzané, France
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Dario Moraga
UMR CNRS 6539-LEMAR (Laboratoire des Sciences de l'Environnement Marin), Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale, Technopôle Brest Iroise, 29280 Plouzané, France
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Edouard Kraffe
UMR CNRS 6539-LEMAR (Laboratoire des Sciences de l'Environnement Marin), Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale, Technopôle Brest Iroise, 29280 Plouzané, France
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  • For correspondence: edouard.kraffe@univ-brest.fr
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SUMMARY

As oxygen concentrations in marine coastal habitats can fluctuate rapidly and drastically, sessile marine organisms such as the oyster Crassostrea gigas can experience marked and rapid oxygen variations. In this study, we investigated the responses of oyster gill mitochondria to short-term hypoxia (3 and 12 h, at 1.7 mg O2 l−1) and subsequent re-oxygenation. Mitochondrial respiratory rates (states 3 and 4 stimulated by glutamate) and phosphorylation efficiency [respiratory control ratio (RCR) and the relationship between ADP and oxygen consumption (ADP/O)] were measured. Cytochrome c oxidase (CCO) activity and cytochrome concentrations (a, b, c1 and c) were measured to investigate the rearrangements of respiratory chain subunits. The potential implication of an alternative oxidase (AOX) was investigated using an inhibitor of the respiratory chain (antimycin A) and through gene expression analysis in gills and digestive gland. Results indicate a downregulation of mitochondrial capacity, with 60% inhibition of respiratory rates after 12 h of hypoxia. RCR remained stable, while ADP/O increased after 12 h of hypoxia and 1 h of re-oxygenation, suggesting increased phosphorylation efficiency. CCO showed a fast and remarkable increase of its catalytic activity only after 3 h of hypoxia. AOX mRNA levels showed similar patterns in gills and digestive gland, and were upregulated after 12 and 24 h of hypoxia and during re-oxygenation. Results suggest a set of controls regulating mitochondrial functions in response to oxygen fluctuations, and demonstrate the fast and extreme plasticity of oyster mitochondria in response to oxygen variations.

FOOTNOTES

  • AUTHOR CONTRIBUTIONS

    R.S., C.F., P.S. and E.K. conceived and designed the experiments; R.S., T.D. and E.K. performed the experiments; R.S. and E.K. analyzed the data; R.S. and E.K. wrote and drafted the paper; and P.S., C.R. and D.M. revised the article.

  • Supplementary material available online at http://jeb.biologists.org/cgi/content/full/216/9/1561/DC1

  • COMPETING INTERESTS

    No competing interests declared.

  • FUNDING

    R.S. was funded through a fellowship from the French Research Ministry (Ministère de l'Enseignement Supérieur et de la Recherche, M.E.S.R.). Funding for the experiment was provided by two projects in Europole Mer (research consortium on marine science and technology in Brittany, France): OxyGenes and LIPIDOMITO.

  • © 2013. Published by The Company of Biologists Ltd
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Keywords

  • Hypoxia
  • Re-oxygenation
  • Oyster
  • Mitochondria
  • Respiration
  • alternative oxidase

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Research Article
Rapid mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oyster, Crassostrea gigas
Rossana Sussarellu, Tony Dudognon, Caroline Fabioux, Philippe Soudant, Dario Moraga, Edouard Kraffe
Journal of Experimental Biology 2013 216: 1561-1569; doi: 10.1242/jeb.075879
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Research Article
Rapid mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oyster, Crassostrea gigas
Rossana Sussarellu, Tony Dudognon, Caroline Fabioux, Philippe Soudant, Dario Moraga, Edouard Kraffe
Journal of Experimental Biology 2013 216: 1561-1569; doi: 10.1242/jeb.075879

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