A novel quinone biosynthetic pathway illuminates the evolution of aerobic metabolism

The dominant organisms in modern oxic ecosystems rely on respiratory quinones with high redox potential (HPQs) for electron transport in aerobic respiration and photosynthesis. The diversification of quinones, from low redox potential (LPQ) in anaerobes to HPQs in aerobes, is assumed to have followed Earth's surface oxygenation ~2.3 billion years ago. However, the evolutionary origins of HPQs remain unresolved. Here, we characterize the structure and biosynthetic pathway of an ancestral HPQ, methyl-plastoquinone (mPQ), that is unique to bacteria of the phylum <i>Nitrospirota</i>. mPQ is structurally related to the two previously known HPQs, plastoquinone from <i>Cyanobacteriota</i>/chloroplasts and ubiquinone from <i>Pseudomonadota</i>/mitochondria, respectively. We demonstrate a common origin of the three HPQ biosynthetic pathways that predates the emergence of <i>Nitrospirota</i>, <i>Cyanobacteriota</i>, and <i>Pseudomonadota</i>. An ancestral HPQ biosynthetic pathway evolved ≥ 3.4 billion years ago in an extinct lineage and was laterally transferred to these three phyla ~2.5 to 3.2 billion years ago. We show that <i>Cyanobacteriota</i> and <i>Pseudomonadota</i> were ancestrally aerobic and thus propose that aerobic metabolism using HPQs significantly predates Earth's surface oxygenation. Two of the three HPQ pathways were later obtained by eukaryotes through endosymbiosis forming chloroplasts and mitochondria, enabling their rise to dominance in modern oxic ecosystems.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2025-02-20
DOI
https://doi.org/10.1073/pnas.2421994122
Citations
20
Primary Topic
Photosynthetic Processes and Mechanisms
Type
article
Field-Weighted Citation Impact
16.12

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article

A novel quinone biosynthetic pathway illuminates the evolution of aerobic metabolism

Vinitra Nathan, Pieter Blom, Eva Spieck, Sebastian Lücker et al.
20 citations
Proceedings of the National Academy of Sciences
Photosynthetic Processes and Mechanisms
16.12
article

A novel quinone biosynthetic pathway illuminates the evolution of aerobic metabolism

Vinitra Nathan, Pieter Blom, Eva Spieck, Sebastian Lücker, Kai‐Uwe Hinrichs, Ludovic Pélosi, Sophie-Carole Chobert, Jared R. Leadbetter, Frauke Baymann, T. Evans, Ahcène Boumendjel, Ann Pearson, Jordon Hemingway, Roger E. Summons, Fabien Pierrel, Sophie S. Abby, Felix J. Elling, Kevin W. Becker, Juliette Schnoebelen, Arthur Reveillard, Julia Cordes
article en
20 citations

Abstract

The dominant organisms in modern oxic ecosystems rely on respiratory quinones with high redox potential (HPQs) for electron transport in aerobic respiration and photosynthesis. The diversification of quinones, from low redox potential (LPQ) in anaerobes to HPQs in aerobes, is assumed to have followed Earth's surface oxygenation ~2.3 billion years ago. However, the evolutionary origins of HPQs remain unresolved. Here, we characterize the structure and biosynthetic pathway of an ancestral HPQ, methyl-plastoquinone (mPQ), that is unique to bacteria of the phylum <i>Nitrospirota</i>. mPQ is structurally related to the two previously known HPQs, plastoquinone from <i>Cyanobacteriota</i>/chloroplasts and ubiquinone from <i>Pseudomonadota</i>/mitochondria, respectively. We demonstrate a common origin of the three HPQ biosynthetic pathways that predates the emergence of <i>Nitrospirota</i>, <i>Cyanobacteriota</i>, and <i>Pseudomonadota</i>. An ancestral HPQ biosynthetic pathway evolved ≥ 3.4 billion years ago in an extinct lineage and was laterally transferred to these three phyla ~2.5 to 3.2 billion years ago. We show that <i>Cyanobacteriota</i> and <i>Pseudomonadota</i> were ancestrally aerobic and thus propose that aerobic metabolism using HPQs significantly predates Earth's surface oxygenation. Two of the three HPQ pathways were later obtained by eukaryotes through endosymbiosis forming chloroplasts and mitochondria, enabling their rise to dominance in modern oxic ecosystems.

Proceedings of the National Academy of SciencesVol. 122(8)
Institut polytechnique de Grenoble (FR), California Institute of Technology (US), Centre National de la Recherche Scientifique (FR), Planetary Science Institute (US), Harvard University (US), Radboud University Nijmegen (NL), Inserm (FR), Universität Hamburg (DE), University of Bremen (DE), Radboud University Medical Center (NL), Christian-Albrechts-Universität zu Kiel (DE), GEOMAR Helmholtz Centre for Ocean Research Kiel (DE), ETH Zurich (CH), Bioénergétique et Ingénierie des Protéines (FR), VetAgro Sup (FR), Radboud Institute for Molecular Life Sciences (NL), Geological Institute (RU), Massachusetts Institute of Technology (US), Université Grenoble Alpes (FR)
National Science Foundation, National Aeronautics and Space Administration, Gordon and Betty Moore Foundation, Alexander von Humboldt-Stiftung, California Institute of Technology, European Commission, Deutsche Forschungsgemeinschaft, Agence Nationale de la Recherche, Eidgenössische Technische Hochschule Zürich, Nederlandse Organisatie voor Wetenschappelijk Onderzoek, Nuclear Safety and Security Commission, NASA Astrobiology Institute, European Research Council
Life in Land
Openalex Percentile: Top 1%
Photosynthetic Processes and Mechanisms
16.12
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