Rooting the Eukaryotic Tree with Mitochondrial and Bacterial Proteins

R Derelle,B F Lang

doi:10.1093/molbev/msr295

Abstract

By exploiting the large body of genome data and the considerable progress in phylogenetic methodology, recent phylogenomic studies have provided new insights into the relationships among major eukaryotic groups. However, confident placement of the eukaryotic root remains a major challenge. This is due to the large evolutionary distance separating eukaryotes from their closest relatives, the Archaea, implying a weak phylogenetic signal and strong long-branch attraction artifacts. Here, we apply a new approach to the rooting of the eukaryotic tree by using a subset of genomic information with more recent evolutionary origin-mitochondrial sequences, whose closest relatives are α-Proteobacteria. For this, we identified and assembled a data set of 42 mitochondrial proteins (mainly encoded by the nuclear genome) and performed Bayesian and maximum likelihood analyses. Taxon sampling includes the recently sequenced Thecamonas trahens, a member of the phylogenetically elusive Apusozoa. This data set confirms the relationships of several eukaryotic supergroups seen before and places the eukaryotic root between the monophyletic "unikonts" and "bikonts." We further show that T. trahens branches sister to Opisthokonta with significant statistical support and question the bikont/excavate affiliation of Malawimonas species. The mitochondrial data set developed here (to be expanded in the future) constitutes a unique alternative means in resolving deep eukaryotic relationships.

Highlights

The morphological and genetic simplicity of amitochondriate protists were previously thought to resemble an ancestral premitochondrial phase of eukaryote evolution
A New Large Multigene Data Set Based on Mitochondrial Proteins Only ten mtDNA-encoded proteins that satisfy our selection criteria for phylogenetic analyses are encoded in the mitochondrial genome of the 15 eukaryotic species considered in our analysis, which is most likely insufficient for rooting the eukaryotic tree
The chosen proteins are present in a wide range of eukaryotes, are clearly orthologs, of a-proteobacterial origin, and as it turns out, all have a predicted mitochondrial localization

Summary

Introduction

The morphological and genetic simplicity of amitochondriate protists (such as diplomonads or microsporidians) were previously thought to resemble an ancestral premitochondrial phase of eukaryote evolution. Species were placed at the base of the eukaryotic tree in a crown-group phylogeny, known as the archezoan scenario (Sogin 1991). It is evident that such lineages evolved from more complex mitochondriate ancestral forms by reductive evolution (Philippe et al 2000; Brinkmann and Philippe 2007) The former placement of the amitochondriate protists at the base of the eukaryotic tree (Baldauf et al 1996; Bapteste et al 2002; Ciccarelli et al 2006; Cox et al 2008) is attributed to long-branch attraction (LBA), a phylogenetic artifact that tends to erroneously group fast-evolving species, as well as attract them to a distant outgroup (Philippe and Germot 2000; Arisue et al 2005; Brinkmann et al 2005). Despite a wealth of molecular data that have become available in the past decade, the root of the phylogenetic tree of eukaryotes remains undefined (Baldauf 2003; Roger and Simpson 2009; Gribaldo et al 2010; Koonin 2010)

Methods

Results

Conclusion