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 R. Knopp; Katharina Trost; Luca Modjewski; Nico Bremer; Marek Mentel; Mauro Degli Esposti; Itzhak Mizrahi; John F. Allen; William F. Martin

doi:https://doi.org/10.1002/1873-3468.14906

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 R. Knopp, Katharina Trost, Luca Modjewski, Nico Bremer, Marek Mentel, Mauro Degli Esposti, Itzhak Mizrahi, John F. Allen, William F. Martin

Department of Life Sciences

Ben-Gurion University of the Negev

Research output: Contribution to journal › Article › peer-review

Abstract

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.

Original language	American English
Pages (from-to)	1692-1714
Number of pages	23
Journal	FEBS Letters
Volume	598
Issue number	14
DOIs	https://doi.org/10.1002/1873-3468.14906
State	Published - 1 Jul 2024

Keywords

aerobic metabolism
evolution of aerobes
evolution of respiration
great oxidation event
lateral gene transfer
oxygen inhibition

All Science Journal Classification (ASJC) codes

Genetics
Molecular Biology
Biophysics
Structural Biology
Biochemistry
Cell Biology

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https://doi.org/10.1002/1873-3468.14906

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Mrnjavac, N., Nagies, F. S. P., Wimmer, J. L. E., Kapust, N., Knopp, M. R., Trost, K., Modjewski, L., Bremer, N., Mentel, M., Esposti, M. D., Mizrahi, I., Allen, J. F., & Martin, W. F. (2024). The radical impact of oxygen on prokaryotic evolution—enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third. FEBS Letters, 598(14), 1692-1714. https://doi.org/10.1002/1873-3468.14906

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title = "The radical impact of oxygen on prokaryotic evolution—enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third",

abstract = "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.",

keywords = "aerobic metabolism, evolution of aerobes, evolution of respiration, great oxidation event, lateral gene transfer, oxygen inhibition",

author = "Natalia Mrnjavac and Nagies, {Falk S.P.} and Wimmer, {Jessica L.E.} and Nils Kapust and Knopp, {Michael R.} and Katharina Trost and Luca Modjewski and Nico Bremer and Marek Mentel and Esposti, {Mauro Degli} and Itzhak Mizrahi and Allen, {John F.} and Martin, {William F.}",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.",

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doi = "https://doi.org/10.1002/1873-3468.14906",

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Mrnjavac, N, Nagies, FSP, Wimmer, JLE, Kapust, N, Knopp, MR, Trost, K, Modjewski, L, Bremer, N, Mentel, M, Esposti, MD, Mizrahi, I, Allen, JF & Martin, WF 2024, 'The radical impact of oxygen on prokaryotic evolution—enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third', FEBS Letters, vol. 598, no. 14, pp. 1692-1714. https://doi.org/10.1002/1873-3468.14906

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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.

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

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JF - FEBS Letters

IS - 14

ER -

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

Abstract

Keywords

All Science Journal Classification (ASJC) codes

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