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.