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The radical impact of oxygen on prokaryotic evolution-enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third.

Natalia MrnjavacFalk S P NagiesJessica L E WimmerNils KapustMichael R KnoppKatharina TrostLuca ModjewskiNico BremerMarek MentelMauro Degli EspostiItzhak MizrahiJohn F AllenWilliam F Martin
Published in: FEBS letters (2024)
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.
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