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

Edmund R R Moody, Tara Mahendrarajah, Nina Dombrowski, James W Clark, Celine Petitjean, Pierre Offre, Gergely J. Szollosi, Anja Spang, Tom Williams

Research output: Contribution to journalArticle (Academic Journal)peer-review

39 Citations (Scopus)
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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 reveals 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 the bacterial Candidate Phyla Radiation (CPR) within Bacteria as the sister group to the Chloroflexota.
Original languageEnglish
Article numbere66695
JournaleLife
Volume11
DOIs
Publication statusAccepted/In press - 7 Feb 2022

Bibliographical note

Funding Information:
This work was supported by the Gordon and Betty Moore Foundation through grant GBMF9741 to TAW, AS, and GJSz. ERRM was supported by a Royal Society Enhancement Award (RGF\EA\180199) to TAW. CP was supported by NERC grant NE/P00251X/1 to TAW. TAW was supported by a Royal Society University Research Fellowship (URF\R\201024). GJSz received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation program under Grant Agreement 714774 and Grant GINOP-2.3.2.-15-2016-00057. AS received funding from the Swedish Research Council (VR starting grant 2016-03559), the NWO-I foundation of the Netherlands Organisation for Scientific Research (WISE fellowship), and the European Research Council (ERC Starting grant 947317, ASymbEL). ND was supported through the WISE fellowship, ERC StG 947317 and GBMF9741 to AS.

Publisher Copyright:
© Moody et al.

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