The evolution of respiratory O 2 /NO reductases: an out-of-the-phylogenetic-box perspective

Abstract

Complex life on our planet crucially depends on strong redox disequilibria afforded by the almost ubiquitous presence of highly oxidizing molecular oxygen. However, the history of O 2 -levels in the atmosphere is complex and prior to the Great Oxidation Event some 2.3 billion years ago, the amount of O 2 in the biosphere is considered to have been extremely low as compared with present-day values. Therefore the evolutionary histories of life and of O 2 -levels are likely intricately intertwined. The obvious biological proxy for inferring the impact of changing O 2 -levels on life is the evolutionary history of the enzyme allowing organisms to tap into the redox power of molecular oxygen, i.e. the bioenergetic O 2 reductases, alias the cytochrome and quinol oxidases. Consequently, molecular phylogenies reconstructed for this enzyme superfamily have been exploited over the last two decades in attempts to elucidate the interlocking between O 2 levels in the environment and the evolution of respiratory bioenergetic processes. Although based on strictly identical datasets, these phylogenetic approaches have led to diametrically opposite scenarios with respect to the history of both the enzyme superfamily and molecular oxygen on the Earth. In an effort to overcome the deadlock of molecular phylogeny, we here review presently available structural, functional, palaeogeochemical and thermodynamic information pertinent to the evolution of the superfamily (which notably also encompasses the subfamily of nitric oxide reductases). The scenario which, in our eyes, most closely fits the ensemble of these non-phylogenetic data, sees the low O 2 -affinity SoxM- (or A-) type enzymes as the most recent evolutionary innovation and the high-affinity O 2 reductases (SoxB or B and cbb 3 or C) as arising independently from NO-reducing precursor enzymes.