An estimate of the deepest branches of the tree of life from ancient vertically-evolving genes

  1. Edmund RR Moody
  2. Tara A Mahendrarajah
  3. Nina Dombrowski
  4. James W Clark
  5. Celine Petitjean
  6. Pierre Offre
  7. Gergely J Szöllősi
  8. Anja Spang  Is a corresponding author
  9. Tom A Williams  Is a corresponding author
  1. University of Bristol, United Kingdom
  2. Royal Netherlands Institute for Sea Research, Netherlands
  3. Eötvös Loránd University, Hungary

Abstract

Core gene phylogenies provide a window into early evolution, but different gene sets and analytical methods have yielded substantially different views of the tree of life. Trees inferred from a small set of universal core genes have typically supported a long branch separating the archaeal and bacterial domains. By contrast, recent analyses of a broader set of non-ribosomal genes have suggested that Archaea may be less divergent from Bacteria, and that estimates of inter-domain distance are inflated due to accelerated evolution of ribosomal proteins along the inter-domain branch. Resolving this debate is key to determining the diversity of the archaeal and bacterial domains, the shape of the tree of life, and our understanding of the early course of cellular evolution. Here, we investigate the evolutionary history of the marker genes key to the debate. We show that estimates of a reduced Archaea-Bacteria (AB) branch length result from inter-domain gene transfers and hidden paralogy in the expanded marker gene set. By contrast, analysis of a broad range of manually curated marker gene datasets from an evenly sampled set of 700 Archaea and Bacteria reveal that current methods likely underestimate the AB branch length due to substitutional saturation and poor model fit; that the best-performing phylogenetic markers tend to support longer inter-domain branch lengths; and that the AB branch lengths of ribosomal and non-ribosomal marker genes are statistically indistinguishable. Furthermore, our phylogeny inferred from the 27 highest-ranked marker genes recovers a clade of DPANN at the base of the Archaea, and places CPR within Bacteria as the sister group to the Chloroflexota.

Data availability

All of the data, including sequence alignments, trees, annotation files, and scripts associated with this manuscript have been deposited in the FigShare repository at DOI: 10.6084/m9.figshare.13395470.

Article and author information

Author details

  1. Edmund RR Moody

    School of Biological Sciences, University of Bristol, Bristol, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8785-5006
  2. Tara A Mahendrarajah

    Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research, Den Burg, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7032-6581
  3. Nina Dombrowski

    Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research, Den Burg, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. James W Clark

    School of Biological Sciences, University of Bristol, Bristol, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Celine Petitjean

    School of Biological Sciences, University of Bristol, Bristol, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Pierre Offre

    Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research, Den Burg, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Gergely J Szöllősi

    Department of Biological Physics, Eötvös Loránd University, Budapest, Hungary
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8556-845X
  8. Anja Spang

    Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research, Den Burg, Netherlands
    For correspondence
    Anja.Spang@nioz.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6518-8556
  9. Tom A Williams

    School of Biological Sciences, University of Bristol, Bristol, United Kingdom
    For correspondence
    tom.a.williams@bristol.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1072-0223

Funding

Gordon and Betty Moore Foundation (GBMF9741)

  • Anja Spang
  • Tom A Williams

Royal Society (RGF\EA\180199)

  • Edmund RR Moody
  • Tom A Williams

Natural Environment Research Council (NE/P00251X/1)

  • Celine Petitjean
  • Tom A Williams

Royal Society (URF\R\201024)

  • Tom A Williams

H2020 European Research Council (714774)

  • Gergely J Szöllősi

H2020 European Research Council (GINOP-2.3.2.-15-2016-00057)

  • Gergely J Szöllősi

Swedish Research Council (2016-03559)

  • Anja Spang

Netherlands Organisation for Scientific Research (WISE Fellowship)

  • Anja Spang

H2020 European Research Council (947317)

  • Anja Spang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Publication history

  1. Received: January 19, 2021
  2. Preprint posted: January 20, 2021 (view preprint)
  3. Accepted: February 7, 2022
  4. Accepted Manuscript published: February 22, 2022 (version 1)
  5. Version of Record published: March 2, 2022 (version 2)

Copyright

© 2022, Moody et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Edmund RR Moody
  2. Tara A Mahendrarajah
  3. Nina Dombrowski
  4. James W Clark
  5. Celine Petitjean
  6. Pierre Offre
  7. Gergely J Szöllősi
  8. Anja Spang
  9. Tom A Williams
(2022)
An estimate of the deepest branches of the tree of life from ancient vertically-evolving genes
eLife 11:e66695.
https://doi.org/10.7554/eLife.66695
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