Evolutionary Changes after Translational Challenges Imposed by Horizontal Gene Transfer.

Stéphanie Bedhomme,Luz M Valero,Ignacio G Bravo,Miquel-Àngel Pujana,Nùria Bonifaci,Dolors Amorós-Moya,Josefa Gonzalez

doi:10.1093/gbe/evz031

Abstract

Genes acquired by horizontal gene transfer (HGT) may provide the recipient organism with potentially new functions, but proper expression level and integration of the transferred genes in the novel environment are not granted. Notably, transferred genes can differ from the receiving genome in codon usage preferences, leading to impaired translation and reduced functionality.Here, we characterize the genomic and proteomic changes undergone during experimental evolution of Escherichia coli after HGT of three synonymous versions, presenting very different codon usage preference, of an antibiotic resistance gene. The experimental evolution was conducted with and without the corresponding antibiotic and the mutational patterns and proteomic profiles after 1,000 generations largely depend on the experimental growth conditions (e.g., mutations in antibiotic off-target genes), and on the synonymous gene version transferred (e.g., mutations in genes responsive to translational stress). The transfer of an exogenous gene extensively modifies the whole proteome, and these proteomic changes are different for the different version of the transferred gene. Additionally, we identified conspicuous changes in global regulators and in intermediate metabolism, confirmed the evolutionary ratchet generated by mutations in DNA repair genes and highlighted the plasticity of bacterial genomes accumulating large and occasionally transient duplications.Our results support a central role of HGT in fuelling evolution as a powerful mechanism promoting rapid, often dramatic genotypic and phenotypic changes. The profound reshaping of the pre-existing geno/phenotype allows the recipient bacteria to explore new ways of functioning, far beyond the mere acquisition of a novel function.

Highlights

Whereas in eukaryotes a large proportion of genetic novelty arises from gene duplications and mutations, an important part of the genetic diversity of prokaryotes is acquired through DNA transfer between species (Ochman et al 2000; Koonin et al 2001; Medini et al 2005; Dagan et al 2008)
Experimental Evolution after Artificial horizontal gene transfer (HGT) Leads to a Diversity of Genetic Changes
We have analyzed in this work the genotypic and proteomic changes occurring on an evolutionary short-time scale after the horizontal acquisition of synonymous versions of an antibiotic resistance gene

Summary

Introduction

Whereas in eukaryotes a large proportion of genetic novelty arises from gene duplications and mutations, an important part of the genetic diversity of prokaryotes is acquired through DNA transfer between species (Ochman et al 2000; Koonin et al 2001; Medini et al 2005; Dagan et al 2008). HGT is the main mechanism of propagation of enzymatic resistance to antibiotics, making it the biological mechanism at the origin of a fundamental public health problem (Martınez et al 2015). Even though it is a successful process from an evolutionary point of view, there are a number of biological and physical barriers to HGT (Thomas and Nielsen 2005).

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