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An archaeal origin of the Wood-Ljungdahl H4MPT branch and the emergence of bacterial methylotrophy

Abstract : The tetrahydromethanopterin (H 4 MPT) methyl branch of the Wood-Ljungdahl pathway is shared by archaeal and bacterial metabolisms that greatly contribute to the global carbon budget and greenhouse gas fluxes: methanogenesis and methylotrophy, including methanotrophy 1-3. It has been proposed that the H 4 MPT branch dates back to the last universal common ancestor 4-6. Interestingly, it has been identified in numerous recently sequenced and mostly uncultured non-methanogenic and non-methylotrophic archaeal and bacterial lineages, where its function remains unclear 5,7. Here, we have examined the distribution and phylogeny of the enzymes involved in the H 4 MPT branch and the biosyn-thesis of its cofactors in over 6,400 archaeal and bacterial genomes. We find that a full Wood-Ljungdahl H 4 MPT pathway is widespread in Archaea and is likely ancestral to this domain, whereas this is not the case for Bacteria. Moreover, the inclusion of recently sequenced lineages leads to an important shortening of the branch separating Archaea and Bacteria with respect to previous phylogenies of the H 4 MPT branch. Finally, the genes for the pathway are colocalized in many of the recently sequenced archaeal lineages, similar to bacteria. Together, these results weaken the last universal common ancestor hypothesis and rather favour an origin of the H 4 MPT branch in Archaea and its subsequent transfer to Bacteria. We propose a scenario for its potential initial role in the first bacterial recipients and its evolution up to the emergence of aerobic methylotrophy. Finally, we discuss how an ancient horizontal transfer not only triggered the emergence of key metabolic processes but also important transitions in Earth's history. The Wood-Ljungdahl (WL) pathway consists of the reversible reduction of CO 2 into the carbonyl and methyl moieties of acetyl-coenzyme A (acetyl-CoA) through two separate (carbonyl and methyl) branches 8 (Fig.
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Panagiotis Adam, Simonetta Gribaldo, Guillaume Borrel. An archaeal origin of the Wood-Ljungdahl H4MPT branch and the emergence of bacterial methylotrophy. Nature Microbiology, Nature Publishing Group, 2019, 4 (12), pp.2155-2163. ⟨10.1038/s41564-019-0534-2⟩. ⟨pasteur-02445428⟩

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