Integrative modeling of gene and genome evolution roots the archaeal tree of life

Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved April 24, 2017 (received for review November 7, 2016)
May 22, 2017
114 (23) E4602-E4611

Significance

The Archaea represent a primary domain of cellular life, play major roles in modern-day biogeochemical cycles, and are central to debates about the origin of eukaryotic cells. However, understanding their origins and evolutionary history is challenging because of the immense time spans involved. Here we apply a new approach that harnesses the information in patterns of gene family evolution to find the root of the archaeal tree and to resolve the metabolism of the earliest archaeal cells. Our approach robustly distinguishes between published rooting hypotheses, suggests that the first Archaea were anaerobes that may have fixed carbon via the Wood–Ljungdahl pathway, and quantifies the cumulative impact of horizontal transfer on archaeal genome evolution.

Abstract

A root for the archaeal tree is essential for reconstructing the metabolism and ecology of early cells and for testing hypotheses that propose that the eukaryotic nuclear lineage originated from within the Archaea; however, published studies based on outgroup rooting disagree regarding the position of the archaeal root. Here we constructed a consensus unrooted archaeal topology using protein concatenation and a multigene supertree method based on 3,242 single gene trees, and then rooted this tree using a recently developed model of genome evolution. This model uses evidence from gene duplications, horizontal transfers, and gene losses contained in 31,236 archaeal gene families to identify the most likely root for the tree. Our analyses support the monophyly of DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaea), a recently discovered cosmopolitan and genetically diverse lineage, and, in contrast to previous work, place the tree root between DPANN and all other Archaea. The sister group to DPANN comprises the Euryarchaeota and the TACK Archaea, including Lokiarchaeum, which our analyses suggest are monophyletic sister lineages. Metabolic reconstructions on the rooted tree suggest that early Archaea were anaerobes that may have had the ability to reduce CO2 to acetate via the Wood–Ljungdahl pathway. In contrast to proposals suggesting that genome reduction has been the predominant mode of archaeal evolution, our analyses infer a relatively small-genomed archaeal ancestor that subsequently increased in complexity via gene duplication and horizontal gene transfer.

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Acknowledgments

T.A.W. is supported by a Royal Society University Research Fellowship. T.M.E. acknowledges support from the European Research Council Advanced Investigator Programme and the Wellcome Trust (Grants ERC- 2010-AdG-268701 and -045404). This work also was supported by grants from the European Research Council (ERC Starting Grant 310039-PUZZLE_CELL), the Swedish Foundation for Strategic Research (Grant SSF-FFL5), and the Swedish Research Council (Grant 2015-04959, to T.J.G.E.). A.S. received Marie Curie Intra-European Fellowship Grant 625521 from the European Union to join the T.J.G.E. laboratory. P.G.F. was supported by the Biotechnology and Biological Resources Sciences Research Council (Grant BB/G024707/1). B.B. was supported by the French Agence Nationale de la Recherche through Grant ANR-10-BINF-01–01, “Ancestrome”. G.J.S. received funding from the European Research Council under the European Union's Horizon 2020 research and innovation programme under Grant Agreement 714774.

Supporting Information

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 114 | No. 23
June 6, 2017
PubMed: 28533395

Classifications

Submission history

Published online: May 22, 2017
Published in issue: June 6, 2017

Keywords

  1. evolution
  2. phylogenetics
  3. Archaea

Acknowledgments

T.A.W. is supported by a Royal Society University Research Fellowship. T.M.E. acknowledges support from the European Research Council Advanced Investigator Programme and the Wellcome Trust (Grants ERC- 2010-AdG-268701 and -045404). This work also was supported by grants from the European Research Council (ERC Starting Grant 310039-PUZZLE_CELL), the Swedish Foundation for Strategic Research (Grant SSF-FFL5), and the Swedish Research Council (Grant 2015-04959, to T.J.G.E.). A.S. received Marie Curie Intra-European Fellowship Grant 625521 from the European Union to join the T.J.G.E. laboratory. P.G.F. was supported by the Biotechnology and Biological Resources Sciences Research Council (Grant BB/G024707/1). B.B. was supported by the French Agence Nationale de la Recherche through Grant ANR-10-BINF-01–01, “Ancestrome”. G.J.S. received funding from the European Research Council under the European Union's Horizon 2020 research and innovation programme under Grant Agreement 714774.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

School of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, United Kingdom;
Gergely J. Szöllősi2
MTA-ELTE Lendület Evolutionary Genomics Research Group, 1117 Budapest, Hungary;
Anja Spang2
Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, SE-75123 Uppsala, Sweden;
Peter G. Foster
Department of Life Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
Sarah E. Heaps
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, United Kingdom;
School of Mathematics & Statistics, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom;
Bastien Boussau
Univ Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558, F-69622 Villeurbanne, France
Thijs J. G. Ettema
Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, SE-75123 Uppsala, Sweden;
T. Martin Embley
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, United Kingdom;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: T.A.W., T.J.G.E., and T.M.E. designed research; T.A.W., G.J.S., A.S., P.G.F., S.E.H., and B.B. performed research; G.J.S. and B.B. contributed new reagents/analytic tools; T.A.W., G.J.S., A.S., P.G.F., S.E.H., and B.B. analyzed data; and T.A.W., A.S., T.J.G.E., and T.M.E. wrote the paper.
2
G.J.S. and A.S. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    Integrative modeling of gene and genome evolution roots the archaeal tree of life
    Proceedings of the National Academy of Sciences
    • Vol. 114
    • No. 23
    • pp. 5761-E4696

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