Abstract

Eukaryotes are typically depicted as descendants of archaea, but their genomes are evolutionary chimeras with genes stemming from archaea and bacteria. Which prokaryotic heritage predominates? Here, we have clustered 19,050,992 protein sequences from 5,443 bacteria and 212 archaea with 3,420,731 protein sequences from 150 eukaryotes spanning six eukaryotic supergroups. By downsampling, we obtain estimates for the bacterial and archaeal proportions. Eukaryotic genomes possess a bacterial majority of genes. On average, the majority of bacterial genes is 56% overall, 53% in eukaryotes that never possessed plastids, and 61% in photosynthetic eukaryotic lineages, where the cyanobacterial ancestor of plastids contributed additional genes to the eukaryotic lineage. Intracellular parasites, which undergo reductive evolution in adaptation to the nutrient rich environment of the cells that they infect, relinquish bacterial genes for metabolic processes. Such adaptive gene loss is most pronounced in the human parasite Encephalitozoon intestinalis with 86% archaeal and 14% bacterial derived genes. The most bacterial eukaryote genome sampled is rice, with 67% bacterial and 33% archaeal genes. The functional dichotomy, initially described for yeast, of archaeal genes being involved in genetic information processing and bacterial genes being involved in metabolic processes is conserved across all eukaryotic supergroups.

Highlights

  • Biologists recognize three kinds of cells in nature: bacteria, archaea and eukaryotes

  • The functional dichotomy, initially described for yeast, of archaeal genes being involved in genetic information processing and bacterial genes being involved in metabolic processes is conserved across all eukaryotic supergroups

  • Using a sample of 5,655 prokaryotic and 150 eukaryotic genomes and downsampling procedures to correct for the overabundance of bacterial genomes versus archaeal genomes for comparisons, we have obtained estimates for the proportion of archaeal and bacterial genes per genome in eukaryotes based on gene distributions

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Summary

Introduction

Biologists recognize three kinds of cells in nature: bacteria, archaea and eukaryotes. The bacteria and archaea are prokaryotic in organization, having generally small cells on the order of 0.5–5 microns in size and ribosomes that translate nascent mRNA molecules as they are synthesized on DNA (cotranscriptional translation) [1]. Eukaryotic cells are generally much larger in size, more complex in organization and have larger genomes possessing introns that are removed (spliced) from the mRNA on spliceosomes [2]. Eukaryotic cells always harbor a system of internal membranes [3,4] that form the endoplasmic reticulum and the cell nucleus, where splicing takes place [5]. Though eukaryotes are younger than prokaryotes, the nature of their phylogenetic relationship(s) to bacteria and archaea remains debated because of differing views about the evolutionary origin of eukaryotic cells

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