Phylogenetic tree of bacteria showing the occurrence of respiratory quinones. Quinones with high redox potential (UQ, PQ, mPQ) occur only in aerobic Nitrospirota, Pseudomonadota, and Cyanobacteriota. Low potential quinones occur in anaerobic Nitrospirota (MK), some Pseudomonadota (MK), and all Cyanobacteriota (PhQ). Asterisks indicate strains in which presence of mPQ has been verified experimentally. See Fig. S11-13 for detailed trees. The maximum-likelihood phylogenetic tree was constructed from 120 concatenated single copy marker proteins (59) of 547 isolate genomes and metagenome-assembled genomes, covering all bacterial phyla, and rooted using the DST group to approximate the bacterial root (60, 61). Quinone occurrences were derived from instrumental analysis of isolates or inferred from the presence of key biosynthesis genes (SI results; Supplementary Datafile S3; including literature data). Phenotype oxytolerance was curated from strain descriptions. Selected classes/orders denoted inside of rings. Selected phyla denoted outside of rings: ACD, Aquificota-Campylobacterota-Deferribacterota; Desulfob ., Desulfobacterota; DST, Deinococcota-Synergistota606 Thermotogota; BA, Bacillota-Actinomycetota; FCB, Fibrobacterota-Chloroflexota-Bacteroidota; Marg., Candidatus Margulisbacteria; Myxoc., Myxococcota; Nitrospin., Nitrospinota; PVC, Planctomycetota608 Verrucomicrobiota-Chlamydiota; Seri., Candidatus Sericytochromatia; Vamp., Vampirovibrionophyceae. Circles indicate ultra-fast bootstrap support ≥95%. — biorxiv.org
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 characterize the structure and biosynthetic pathway of a novel ancestral HPQ, methyl-plastoquinone, that is unique to bacteria of the phylum Nitrospirota. Methyl-plastoquinone 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 ~2.5-3.2 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.
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