Dynamic quinone repertoire accompanied the diversification of energy metabolism in Pseudomonadota

It is currently unclear how Pseudomonadota, a phylum that originated around the time of the Great Oxidation Event, became one of the most abundant and diverse bacterial phyla on Earth, with metabolically versatile members colonizing a wide range of environments with different O2 concentrations. Here, we address this question by studying isoprenoid quinones, which are central components of energy metabolism covering a wide range of redox potentials. We demonstrate that a dynamic repertoire of quinone biosynthetic pathways accompanied the diversification of Pseudomonadota. The low potential menaquinone (MK) was lost in an ancestor of Pseudomonadota while the high potential ubiquinone (UQ) emerged. We show that the O2-dependent and O2-independent UQ pathways were both present in the last common ancestor of Pseudomonadota, and transmitted vertically. The O2-independent pathway has a conserved genetic organization and displays signs of positive regulation by the master regulator “fumarate and nitrate reductase” (FNR), suggesting a conserved role for UQ in anaerobiosis across Pseudomonadota. The O2-independent pathway was lost in some lineages but maintained in others, where it favoured a secondary reacquisition of low potential quinones (MK or rhodoquinone), which promoted diversification towards aerobic facultative and anaerobic metabolisms. Our results support that the ecological success of Pseudomonadota is linked to the acquisition of the largest known repertoire of quinones, which allowed adaptation to oxic niches as O2 levels increased on Earth, and subsequent diversification into anoxic or O2-fluctuating environments.