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.