TY - JOUR
T1 - The radical impact of oxygen on prokaryotic evolution—enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third
AU - Mrnjavac, Natalia
AU - Nagies, Falk S.P.
AU - Wimmer, Jessica L.E.
AU - Kapust, Nils
AU - Knopp, Michael R.
AU - Trost, Katharina
AU - Modjewski, Luca
AU - Bremer, Nico
AU - Mentel, Marek
AU - Esposti, Mauro Degli
AU - Mizrahi, Itzhak
AU - Allen, John F.
AU - Martin, William F.
N1 - Publisher Copyright:
© 2024 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
PY - 2024/7/1
Y1 - 2024/7/1
N2 - Molecular oxygen is a stable diradical. All O2-dependent enzymes employ a radical mechanism. Generated by cyanobacteria, O2 started accumulating on Earth 2.4 billion years ago. Its evolutionary impact is traditionally sought in respiration and energy yield. We mapped 365 O2-dependent enzymatic reactions of prokaryotes to phylogenies for the corresponding 792 protein families. The main physiological adaptations imparted by O2-dependent enzymes were not energy conservation, but novel organic substrate oxidations and O2-dependent, hence O2-tolerant, alternative pathways for O2-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 O2-containing environments, a prerequisite for the later emergence of aerobic respiratory chains.
AB - Molecular oxygen is a stable diradical. All O2-dependent enzymes employ a radical mechanism. Generated by cyanobacteria, O2 started accumulating on Earth 2.4 billion years ago. Its evolutionary impact is traditionally sought in respiration and energy yield. We mapped 365 O2-dependent enzymatic reactions of prokaryotes to phylogenies for the corresponding 792 protein families. The main physiological adaptations imparted by O2-dependent enzymes were not energy conservation, but novel organic substrate oxidations and O2-dependent, hence O2-tolerant, alternative pathways for O2-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 O2-containing environments, a prerequisite for the later emergence of aerobic respiratory chains.
KW - aerobic metabolism
KW - evolution of aerobes
KW - evolution of respiration
KW - great oxidation event
KW - lateral gene transfer
KW - oxygen inhibition
UR - http://www.scopus.com/inward/record.url?scp=85193380532&partnerID=8YFLogxK
U2 - 10.1002/1873-3468.14906
DO - 10.1002/1873-3468.14906
M3 - Article
C2 - 38750628
AN - SCOPUS:85193380532
SN - 0014-5793
VL - 598
SP - 1692
EP - 1714
JO - FEBS Letters
JF - FEBS Letters
IS - 14
ER -