Oxygen context and relative origins of quinones biosynthetic pathways – QUINEVOL

By provoking a shift from globally reducing to oxidizing conditions on Earth’s surface, the great oxidation event (GOE) had a profound impact on the bioenergetics of ancestral microorganisms. Curiously, in spite of their crucial role in bioenergetics processes, the nearly-universal quinone molecules have been overlooked in the context of O2 rise on Earth. This is the topic of the QUINEVOL project.
Quinones are central to cellular energy production, and have been subject to intense evolutionary pressures provoked by the GOE. Low-potential quinones, which are widely spread and thought to be ancestral, are sensitive to O2 as they quickly get oxidized when O2 levels rise. High-potential quinones are thought to have appeared in response to increased O2 levels. They are found in two lineages that remarkably succeeded in their colonization of oxic environments: the oxygenic Cyanobacteria and Proteobacteria.
Cyanobacteria are considered to be responsible for the GOE as they use oxygenic photosynthesis to generate cellular energy, a process that releases O2 and involves the high-potential quinone plastoquinone (PQ). Until now, Proteobacteria were thought to have emerged after oxygenic Cyanobacteria, as they required O2 to synthetize their essential high-potential quinone ubiquinone (UQ).
Recent discoveries by our team however leads to reconsider the relative timing of appearance of high-potential quinones, and of the organisms that adopted them. We found 1) a very widespread pathway in Proteobacteria that does not require O2 for UQ production and can be involved in anaerobic processes; 2) that the pathway for PQ production in Cyanobacteria requires O2 in at least one of its steps. Moreover, uncertainties on the tempo of Earth’s oxygenation, and the recent discovery of new lineages – including non-oxygenic Cyanobacteria – further question the O2-context of Proteobacteria and Cyanobacteria emergence, and their relative timing of origins.
In the QUINEVOL project, we propose to tackle these questions by performing an unprecedented integrative study of the evolution of quinone biosynthetic pathways. This will allow to shed lights on ancestral microorganisms’ adaptation to rising O2 levels, from a bioenergetics perspective. We propose to 1) design annotation tools to identify quinone biosynthetic pathways in genomes, 2) revise the classical divide between low-potential/high-potential quinones and the environmental conditions they are used in, 3) decipher how UQ and PQ appeared in Proteobacteria and Cyanobacteria respectively, and 4) build a global scenario for quinone evolutionary origins in the context of Earth’s oxygenation.
We propose to use an original combination of phylogenomic and experimental approaches. a) The developed annotation tools will be validated based on text mining approaches on the existing literature and based on experimental characterization of quinones from unexplored Bacterial lineages. This will enable to re-assess the quinones’ repertoire for the “new Tree of Life” while proposing candidate enzymes for missing steps in quinones’ pathways. b) Quinones’ ecophysiology will be re-evaluated using a meta-analysis of the environmental distribution of quinones, and the analysis of an original environmental dataset that will combine lipidomics and metagenomics data. c) A global timed-scenario for quinones’ origins will be built by combining classical phylogenetic analyses with the use of lateral gene transfers events as tools for “molecular dating”. Overall, the original approaches of the QUINEVOL project will enable to shed new lights on adaptations of bioenergetics processes in relation to Earth’s oxygenation.