Article

The physiology and habitat of the last universal common ancestor

  • Nature Microbiology 1, Article number: 16116 (2016)
  • doi:10.1038/nmicrobiol.2016.116
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Abstract

The concept of a last universal common ancestor of all cells (LUCA, or the progenote) is central to the study of early evolution and life's origin, yet information about how and where LUCA lived is lacking. We investigated all clusters and phylogenetic trees for 6.1 million protein coding genes from sequenced prokaryotic genomes in order to reconstruct the microbial ecology of LUCA. Among 286,514 protein clusters, we identified 355 protein families (0.1%) that trace to LUCA by phylogenetic criteria. Because these proteins are not universally distributed, they can shed light on LUCA's physiology. Their functions, properties and prosthetic groups depict LUCA as anaerobic, CO2-fixing, H2-dependent with a Wood–Ljungdahl pathway, N2-fixing and thermophilic. LUCA's biochemistry was replete with FeS clusters and radical reaction mechanisms. Its cofactors reveal dependence upon transition metals, flavins, S-adenosyl methionine, coenzyme A, ferredoxin, molybdopterin, corrins and selenium. Its genetic code required nucleoside modifications and S-adenosyl methionine-dependent methylations. The 355 phylogenies identify clostridia and methanogens, whose modern lifestyles resemble that of LUCA, as basal among their respective domains. LUCA inhabited a geochemically active environment rich in H2, CO2 and iron. The data support the theory of an autotrophic origin of life involving the Wood–Ljungdahl pathway in a hydrothermal setting.

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Acknowledgements

The authors thank J. Baross and N. Lane for discussions. The authors acknowledge the Zentrum für Informations- und Medientechnologie (ZIM) of the Heinrich-Heine University for computational support and the European Research Council for funding (ERC AdG 666053 to W.F.M.).

Author information

Author notes

    • Madeline C. Weiss
    •  & Filipa L. Sousa

    These authors contributed equally to this work.

Affiliations

  1. Institute of Molecular Evolution, Heinrich Heine University Düsseldorf, Universitätsstraße 1, 40225 Düsseldorf, Germany

    • Madeline C. Weiss
    • , Filipa L. Sousa
    • , Natalia Mrnjavac
    • , Sinje Neukirchen
    • , Mayo Roettger
    • , Shijulal Nelson-Sathi
    •  & William F. Martin

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Contributions

M.C.W., F.L.S., S.N., M.R. and S.N.-S. performed the bioinformatics analysis. F.L.S. and N.M. carried out the functional classification of the protein families. All authors analysed and discussed the results. W.F.M., F.L.S. and S.N.-S. designed the research. M.C.W., F.L.S., S.N., N.M., S.N.-S. and W.F.M. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to William F. Martin.

Supplementary information

PDF files

  1. 1.

    Supplementary information

    Supplementary Figures 1-3, Supplementary Tables 1,3-6, legends for Supplementary Tables 2,7-9, Supplementary References

Excel files

  1. 1.

    Supplementary Table 2

    Functional and taxonomic characterization of the 355 protein families potentially present in LUCA using a threshold of 25% global identity

  2. 2.

    Supplementary Table 7

    SAM-dependent enzymes

  3. 3.

    Supplementary Table 8

    Functional and taxonomic characterization of one-taxa-misplaced protein families

  4. 4.

    Supplementary Table 9

    Functional and taxonomic characterization of one-phyla-misplaced protein families