Abstract

The identification of the asgard archaea has fueled speculations regarding the nature of the archaeal host in eukaryogenesis and its level of complexity prior to endosymbiosis. Here, we analyzed the coding capacity of 150 eukaryotes, 1,000 bacteria, and 226 archaea, including the only cultured member of the asgard archaea. Clustering methods that consistently recover endosymbiotic contributions to eukaryotic genomes recover an asgard archaeal-unique contribution of a mere 0.3% to protein families present in the last eukaryotic common ancestor, while simultaneously suggesting that this group’s diversity rivals that of all other archaea combined. The number of homologs shared exclusively between asgard archaea and eukaryotes is only 27 on average. This tiny asgard archaeal-unique contribution to the root of eukaryotic protein families questions claims that archaea evolved complexity prior to eukaryogenesis. Genomic and cellular complexity remains a eukaryote-specific feature and is best understood as the archaeal host’s solution to housing an endosymbiont.

Highlights

  • Four billion years of prokaryotic evolution has only once resulted in the emergence of highly compartmentalized cells and eventually macroscopic body plans: following the origin of eukaryotes through endosymbiosis

  • In order to evaluate to what degree asgard archaea bridge the prokaryotic and eukaryotic protein families, we performed a global comparison of clustered gene families across 11 asgard archaeal metagenome-assembled genomes (MAGs), the closed MAG of the cultured asgard archaeon Candidatus P. syntrophicum MK-D1, 214 other archaea, 1,000 bacteria, and 150 eukaryotes

  • The eukaryote and prokaryote clusters (EPCs) were merged in a reciprocal best cluster approach previously described in Ku et al (2015), yielding EPCs

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Summary

Introduction

Four billion years of prokaryotic evolution has only once resulted in the emergence of highly compartmentalized cells and eventually macroscopic body plans: following the origin of eukaryotes through endosymbiosis. The analysis of core eukaryotic features such as the nucleus, mitochondria, sex and meiosis, compartmentalization and dynamic membrane trafficking, and virtually all of the associated protein families, consistently point to their presence in the last eukaryotic common ancestor (LECA) (Fritz-Laylin et al 2010; Koonin et al 2013; Koumandou et al 2013; Garg and Martin 2016).

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