Formation of chimeric genes with essential functions at the origin of eukaryotes

Raphaël Méheust,Eric Bapteste,Philippe Lopez,Debashish Bhattacharya,Jananan S Pathmanathan,James O Mcinerney

doi:10.1186/s12915-018-0500-0

Abstract

BackgroundEukaryotes evolved from the symbiotic association of at least two prokaryotic partners, and a good deal is known about the timings, mechanisms, and dynamics of these evolutionary steps. Recently, it was shown that a new class of nuclear genes, symbiogenetic genes (S-genes), was formed concomitant with endosymbiosis and the subsequent evolution of eukaryotic photosynthetic lineages. Understanding their origins and contributions to eukaryogenesis would provide insights into the ways in which cellular complexity has evolved.ResultsHere, we show that chimeric nuclear genes (S-genes), built from prokaryotic domains, are critical for explaining the leap forward in cellular complexity achieved during eukaryogenesis. A total of 282 S-gene families contributed solutions to many of the challenges faced by early eukaryotes, including enhancing the informational machinery, processing spliceosomal introns, tackling genotoxicity within the cell, and ensuring functional protein interactions in a larger, more compartmentalized cell. For hundreds of S-genes, we confirmed the origins of their components (bacterial, archaeal, or generally prokaryotic) by maximum likelihood phylogenies. Remarkably, Bacteria contributed nine-fold more S-genes than Archaea, including a two-fold greater contribution to informational functions. Therefore, there is an additional, large bacterial contribution to the evolution of eukaryotes, implying that fundamental eukaryotic properties do not strictly follow the traditional informational/operational divide for archaeal/bacterial contributions to eukaryogenesis.ConclusionThis study demonstrates the extent and process through which prokaryotic fragments from bacterial and archaeal genes inherited during eukaryogenesis underly the creation of novel chimeric genes with important functions.

Highlights

Eukaryotes evolved from the symbiotic association of at least two prokaryotic partners, and a good deal is known about the timings, mechanisms, and dynamics of these evolutionary steps
It has recently been demonstrated that endosymbiosis and the subsequent evolution of eukaryotic photosynthetic lineages was concomitant with the formation of a novel class of nuclear genes, referred to as symbiogenetic genes (S-genes) [1]
We compared all sequences by BLAST [30], using sequence similarity to generate clusters that were considered as gene families

Summary

Introduction

Eukaryotes evolved from the symbiotic association of at least two prokaryotic partners, and a good deal is known about the timings, mechanisms, and dynamics of these evolutionary steps. It was shown that a new class of nuclear genes, symbiogenetic genes (S-genes), was formed concomitant with endosymbiosis and the subsequent evolution of eukaryotic photosynthetic lineages. Understanding their origins and contributions to eukaryogenesis would provide insights into the ways in which cellular complexity has evolved. It has recently been demonstrated that endosymbiosis and the subsequent evolution of eukaryotic photosynthetic lineages was concomitant with the formation of a novel class of nuclear genes, referred to as symbiogenetic genes (S-genes) [1]. Even though the details of the genetic, physiological, and structural basis of their merger remain to be established [13, 14], there is a consensus forming that eukaryotes are a genetic chimera because

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