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

Nature Microbiology volume 4, pages 2155–2163 (2019)Cite this article

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Abstract

The tetrahydromethanopterin (H4MPT) 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 methanotrophy1,2,3. It has been proposed that the H4MPT branch dates back to the last universal common ancestor4,5,6. 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 unclear5,7. Here, we have examined the distribution and phylogeny of the enzymes involved in the H4MPT branch and the biosynthesis of its cofactors in over 6,400 archaeal and bacterial genomes. We find that a full Wood–Ljungdahl H4MPT 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 H4MPT 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 H4MPT 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.

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Fig. 1: Schematic of the WL pathway reactions and their relationships with other methylotrophy modules.
Fig. 2: Phylogenomic and synteny data supporting the transfer of the H4MPT branch and its cofactor biosynthesis.
Fig. 3: Scenario for the origin and evolution of the H4MPT methyl branch in Bacteria.
Fig. 4: Metabolic prediction of Limitata with main biochemical reactions.

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Data availability

All raw data (HMM profiles, initial and trimmed alignments, and full trees in Newick format) are available in Supplementary Data 4.

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Acknowledgements

P.S.A. is supported by a PhD fellowship from Université Paris Diderot and by funds from the PhD Programme ‘Frontières du Vivant (FdV)–Programme Bettencourt’. G.B. acknowledges support from the Institut Pasteur through a Roux–Cantarini fellowship. S.G. acknowledges funding from the French National Agency for Research Grant ArchEvol (ANR-16-CE02-0005-01).

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  1. Panagiotis S. Adam

    Present address: Group for Aquatic Microbial Ecology, Biofilm Centre, Faculty of Chemistry, University of Duisburg-Essen, Essen, Germany

Authors and Affiliations

  1. Department of Microbiology, Unit Evolutionary Biology of the Microbial Cell, Institut Pasteur, Paris, France

    Panagiotis S. Adam, Guillaume Borrel & Simonetta Gribaldo

  2. Université Paris Diderot, Sorbonne Paris Cité, Paris, France

    Panagiotis S. Adam

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Contributions

S.G. and P.S.A. designed the research. P.S.A. performed all phylogenomic analyses. P.S.A. and G.B. performed the genome synteny and metabolic reconstruction analyses. P.S.A., G.B. and S.G. analysed the data and wrote the paper.

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Correspondence to Simonetta Gribaldo.

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Supplementary Information

Supplementary Information

Supplementary Figs. 1–22, Supplementary zip file legend and Supplementary legends.

Reporting Summary

Supplementary Data 1

Accession numbers for utilized sequences.

Supplementary Data 2

Metabolic annotations of Limitata genomes.

Supplementary Data 3

Names and taxon IDs of taxa used to construct the local databank of bacterial and archaeal genomes.

Supplementary Data 4

HMM profiles for each gene used in this work for Archaea and Bacteria; initial and post-trimming multiple sequence alignments used to generate the phylogenies presented in this work; Newick files corresponding to each phylogeny presented in this work.

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Adam, P.S., Borrel, G. & Gribaldo, S. An archaeal origin of the Wood–Ljungdahl H4MPT branch and the emergence of bacterial methylotrophy. Nat Microbiol 4, 2155–2163 (2019). https://doi.org/10.1038/s41564-019-0534-2

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