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

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 not be very 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, which act to artifactually diminish the genetic distance between the two domains. By contrast, analysis of a broad range of manually curated marker gene datasets from a sample 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. A phylogeny of prokaryotes inferred from the 27 highest-ranked marker genes, including ribosomal and non-ribosomal markers, supported a long AB branch, recovered a clade of DPANN at the base of the Archaea, and placed CPR within Bacteria as the sister group to the Chloroflexota.