Reversed electron transfer through the bc1complex enables a cytochrome c oxidase mutant (Δaa3/cbb3) ofParacoccus denitrificansto grow on methylamine

Abstract

In Paracoccus denitrificans four classes of redox proteins are involved in the electron transfer from methylamine to oxygen: methylamine dehydrogenase (MADH), amicyanin, cytochrome c and cytochrome c oxidase. MADH and its electron acceptor amicyanin are indispensable for growth on methylamine. At least three different cytochromes c and two types of cytochrome c oxidase, cytochromes aa ₃ and cbb ₃, have previously been proposed to participate in the electron transfer pathways from methylamine to oxygen. In this study, participation of both cytochrome c oxidases and of the quinol oxidase (cytochrome bb ₃) has indeed been confirmed by analysis of a series of oxidase mutants. Interestingly, a P. denitrificans cytochrome c oxidase mutant (Δ aa ₃/cbb ₃) retains the capacity to oxidise methylamine. It is demonstrated that the oxidation of the cytochrome c pool in this mutant does not proceed via an alternative cytochrome c oxidase, but rather via an ‘uphill’ electron transfer through the bc ₁ complex to ubiquinone, driven by the membrane potential. The subsequent oxidation of ubiquinol proceeds via the only remaining terminal oxidase, the bb ₃‐type quinol oxidase.