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 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 reconstruct the biosynthetic pathway of a novel HPQ, methyl-plastoquinone, that is unique to bacteria of the phylum Nitrospirota.

We demonstrate that the three extant HPQ biosynthetic pathways, in Nitrospirota, Cyanobacteriota, and Pseudomonadota, share a common origin that predates the emergence of these phyla.

We show that aerobic metabolism using HPQs is ancestral to Cyanobacteriota and Pseudomonadota and significantly predates Earth’s surface oxygenation.

Characterization of the mPQ biosynthetic pathway. a, Biosynthetic pathways of quinones showing homology of pathways for mPQ9 in Nitrospirota (purple), PQ9 in the cyanobacterium Synechocystis sp. PCC6803 (green) and UQ8 in the gammaproteobacterium Escherichia coli (blue). Biosynthetic steps are numbered, and homologous steps are connected by colored lines. b-d, Heterologous complementation experiments using mPQ biosynthesis gene candidates to restore UQ8 production in E. coli mutants lacking key genes for ubiquinone biosynthesis (∆ubiC+mpqC, ∆ubiA+mpqA, ∆ubiX+mpqX, ∆ubiD+mpqD). e, PQ production in E. coli ∆ubiIFE mutants complemented with mpqQ from N. inopinata as well as PQ and mPQ in E. coli ∆ubiIFE mutants complemented with mpqQ from N. inopinata and mpqE from other Nitrospirota. WT=wild type; vec=empty vector; thick bars represent means and error bars represent standard deviations of the means, n=3-5; AU=arbitrary units. Abbreviations: Ca. N. nitrificans (Nnit), N. moscoviensis (Nmos), N. inopinata (Nino), L. ferrooxidans (Lfer), Ca. M. noduliformans (Mnod). The numbering of the carbon atoms on the 4-HBA precursor (panel a, light grey) defines the nomenclature for all intermediates described in the text. The octaprenyl and nonaprenyl chains are abbreviated with R8 and R9, respectively. See Fig. S7-S9 for details on compound identification and quantification. Stars indicate p < 0.01 (*), p < 0.001 (), and p < 0.0001 () for unpaired Student’s t tests relative to the empty vector. — biorxiv.org

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

A novel quinone biosynthetic pathway illuminates the evolution of aerobic metabolism, biorxiv.org

Astrobiology,