The radical impact of oxygen on prokaryotic evolution—enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third
Natalia Mrnjavac, Falk S. P. Nagies, Jessica L. E. Wimmer, Nils Kapust, Michael Knopp, Katharina Trost, Luca Modjewski, Nico Bremer, Marek Mentel, Mauro Degli Esposti, Itzhak Mizrahi, John F. Allen, William Martin
Abstract
Molecular oxygen is a stable diradical. All O 2 ‐dependent enzymes employ a radical mechanism. Generated by cyanobacteria, O 2 started accumulating on Earth 2.4 billion years ago. Its evolutionary impact is traditionally sought in respiration and energy yield. We mapped 365 O 2 ‐dependent enzymatic reactions of prokaryotes to phylogenies for the corresponding 792 protein families. The main physiological adaptations imparted by O 2 ‐dependent enzymes were not energy conservation, but novel organic substrate oxidations and O 2 ‐dependent, hence O 2 ‐tolerant, alternative pathways for O 2 ‐inhibited reactions. Oxygen‐dependent enzymes evolved in ancestrally anaerobic pathways for essential cofactor biosynthesis including NAD + , pyridoxal, thiamine, ubiquinone, cobalamin, heme, and chlorophyll. These innovations allowed prokaryotes to synthesize essential cofactors in O 2 ‐containing environments, a prerequisite for the later emergence of aerobic respiratory chains.