In the slime mold Dictyostelium discoideum, the subunit composition of cytochrome c oxidase depends on oxygen that inversely regulates the concentrations of two alternative isoforms of the smallest enzyme subunit (Schiavo, G., and Bisson, R.(1989) J. Biol. Chem. 264, 7129-7134). In order to investigate their role in the Dictyostelium life cycle, the expression of the oxidase subunits was monitored during cell growth and development. The results obtained demonstrate that exponentially growing amoebae respond rapidly and precisely to hypoxia by switching the expression of the two isoforms and also by increasing the levels of the mRNAs of the different oxidase subunits in a highly coordinated process. During normal development the ``hypoxic'' subunit is not synthesized, but its level of expression appears to parallel the sensitivity to oxygen of development, rising steeply below 10% oxygen when the differentiation program is virtually blocked. Under these conditions, the expression of the alternative subunit isoform is essentially oxygen-insensitive. These findings suggest that the physiological relevance of the subunit switching concerns primarily the vegetative phase of growth, possibly as part of a more general mechanism evolved in order to evade conditions that do not allow development. Taken together, the data obtained offer an intriguing example of the fine control exerted on the expression of a key respiratory enzyme in a strictly aerobic organism.

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