Apparent redundancy of electron transfer pathways via bc1 complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans

Acidithiobacillus ferrooxidans is an acidophilic chemolithoautotrophic bacterium that can grow in the presence of either the weak reductant Fe2+, or reducing sulfur compounds that provide more energy for growth than Fe2+. We have previously shown that the uphill electron transfer pathway between Fe2+ and NAD(+) involved a bc(1) complex that functions only in the reverse direction [J. Bacteriol. 182, (2000) 3602]. In the present work, we demonstrate both the existence of a bc(1) complex functioning in the forward direction, expressed when the cells are grown on sulfur, and the presence of two terminal oxidases, a bd and a ba(3) type oxidase expressed more in sulfur than in iron-grown cells, besides the cytochrome aa(3) that was found to be expressed only in iron-grown cells. Sulfur-grown cells exhibit a branching point for electron flow at the level of the quinol pool leading on the one hand to a bd type oxidase, and on the other hand to a bc(1) --> ba(3) pathway. We have also demonstrated the presence in the genome of transcriptionally active genes potentially encoding the subunits of a bo(3) type oxidase. A scheme for the electron transfer chains has been established that shows the existence of multiple respiratory routes to a single electron acceptor O-2. Possible reasons for these apparently redundant pathways are discussed. (C) 2004 Elsevier B.V. All rights reserved.