| Title: |
A novel quinone biosynthetic pathway illuminates the evolution of aerobic metabolism |
| Authors: |
Elling, Felix, J; Pierrel, Fabien; Chobert, Sophie-Carole; Abby, Sophie, S; Evans, Thomas, W; Reveillard, Arthur; Pelosi, Ludovic; Schnoebelen, Juliette; Hemingway, Jordon, D; Boumendjel, Ahcène; Becker, Kevin, W; Blom, Pieter; Cordes, Julia; Nathan, Vinitra; Baymann, Frauke; Lücker, Sebastian; Spieck, Eva; Leadbetter, Jared, R; Hinrichs, Kai-Uwe; Summons, Roger, E; Pearson, Ann |
| Contributors: |
Christian-Albrechts-Universität zu Kiel = Christian-Albrechts University of Kiel = Université Christian-Albrechts de Kiel (CAU); Translational microbial Evolution and Engineering (TIMC-TrEE); Translational Innovation in Medicine and Complexity / Recherche Translationnelle et Innovation en Médecine et Complexité - UMR 5525 (TIMC); VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP); Université Grenoble Alpes (UGA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP); Université Grenoble Alpes (UGA); University of Glasgow; Radiopharmaceutiques biocliniques (LRB); Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Grenoble Alpes (UGA); Helmholtz Centre for Ocean Research Kiel (GEOMAR); Radboud University Nijmegen; Zentrum für Marine Umweltwissenschaften Bremen (MARUM); Universität Bremen Deutschland = University of Bremen Germany = Université de Brême Allemagne; Bioénergétique et Ingénierie des Protéines (BIP); Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS); Universität Hamburg = University of Hamburg (UHH); Massachusetts Institute of Technology (MIT); Harvard University; ANR-21-CE02-0018,QUINEVOL,Contexte en oxygène et origine relative des voies de biosynthèse des quinones(2021) |
| Source: |
ISSN: 0027-8424. |
| Publisher Information: |
CCSD; National Academy of Sciences |
| Publication Year: |
2025 |
| Collection: |
Université Grenoble Alpes: HAL |
| Subject Terms: |
[SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry; Molecular Biology/Biochemistry [q-bio.BM]; [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology |
| Description: |
International audience ; 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 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 ~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. |
| Document Type: |
article in journal/newspaper |
| Language: |
English |
| DOI: |
10.1073/pnas.2421994122 |
| Availability: |
https://hal.science/hal-04679398; https://hal.science/hal-04679398v2/document; https://hal.science/hal-04679398v2/file/mPQ_main_20241213.pdf; https://doi.org/10.1073/pnas.2421994122 |
| Rights: |
https://creativecommons.org/licenses/by-nc-nd/4.0/ ; info:eu-repo/semantics/OpenAccess |
| Accession Number: |
edsbas.4362160F |
| Database: |
BASE |