A novel quinone biosynthetic pathway illuminates the evolution of aerobic metabolism

• 成果类型: Article
• 署名作者: Elling, Felix J.; Pierrel, Fabien; Chobert, Sophie-Carole; Abby, Sophie S.; Evans, Thomas W.; Reveillard, Arthur; Pelosi, Ludovic; Schnoebelen, Juliette; Hemingway, Jordon D.; Boumendjel, Ahcene; Becker, Kevin W.; Blom, Pieter; Cordes, Julia; Nathan, Vinitra; Baymann, Frauke; Lucker, Sebastian; Spieck, Eva; Leadbetter, Jared R.; Hinrichs, Kai-Uwe; Summons, Roger E.; Pearson, Ann
• 署名单位: Harvard University; University of Kiel; VetAgro Sup; Communaute Universite Grenoble Alpes; Institut National Polytechnique de Grenoble; Universite Grenoble Alpes (UGA); Centre National de la Recherche Scientifique (CNRS); CNRS - Institute for Engineering & Systems Sciences (INSIS); Massachusetts Institute of Technology (MIT); University of Bremen; University of Bremen; Swiss Federal Institutes of Technology Domain; ETH Zurich; Institut National de la Sante et de la Recherche Medicale (Inserm); Communaute Universite Grenoble Alpes; Universite Grenoble Alpes (UGA); Helmholtz Association; GEOMAR Helmholtz Center for Ocean Research Kiel; Radboud University Nijmegen; Aix-Marseille Universite; Centre National de la Recherche Scientifique (CNRS); University of Hamburg; California Institute of Technology; California Institute of Technology; Royal Dutch Shell; Boston University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-10158
• DOI: 10.1073/pnas.2421994122
• 发表日期: 2025-02-25
• 关键词: menaquinone biosynthesis; oxygen; identification; plastoquinone; cyanobacteria; oxidation; bacterial; LIFE; methyltransferases; physiology

摘要

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 similar to 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, methylplastoquinone (mPQ), that is unique to bacteria of the phylum Nitrospirota. mPQ is structurally related to the two previously known HPQs, plastoquinone from Cyanobacteriota/chloroplasts and ubiquinone from Pseudomonadota/mitochondria, respectively. We demonstrate a common origin of the three HPQ biosynthetic pathways that predates the emergence of Nitrospirota, Cyanobacteriota, and Pseudomonadota. An ancestral HPQ biosynthetic pathway evolved >= 3.4 billion years ago in an extinct lineage and was laterally transferred to these three phyla similar to 2.5 to 3.2 billion years ago. We show that Cyanobacteriota and Pseudomonadota 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.