Trade-Offs of Escherichia coli Adaptation to an Intracellular Lifestyle in Macrophages

PLoS One. 2016 Jan 11;11(1):e0146123. doi: 10.1371/journal.pone.0146123. eCollection 2016.

Abstract

The bacterium Escherichia coli exhibits remarkable genomic and phenotypic variation, with some pathogenic strains having evolved to survive and even replicate in the harsh intra-macrophage environment. The rate and effects of mutations that can cause pathoadaptation are key determinants of the pace at which E. coli can colonize such niches and become pathogenic. We used experimental evolution to determine the speed and evolutionary paths undertaken by a commensal strain of E. coli when adapting to intracellular life. We estimated the acquisition of pathoadaptive mutations at a rate of 10-6 per genome per generation, resulting in the fixation of more virulent strains in less than a hundred generations. Whole genome sequencing of independently evolved clones showed that the main targets of intracellular adaptation involved loss of function mutations in genes implicated in the assembly of the lipopolysaccharide core, iron metabolism and di- and tri-peptide transport, namely rfaI, fhuA and tppB, respectively. We found a substantial amount of antagonistic pleiotropy in evolved populations, as well as metabolic trade-offs, commonly found in intracellular bacteria with reduced genome sizes. Overall, the low levels of clonal interference detected indicate that the first steps of the transition of a commensal E. coli into intracellular pathogens are dominated by a few pathoadaptive mutations with very strong effects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological* / drug effects
  • Adaptation, Physiological* / genetics
  • Animals
  • Biological Evolution
  • Clone Cells
  • Escherichia coli / drug effects
  • Escherichia coli / growth & development
  • Escherichia coli / physiology*
  • Escherichia coli Proteins / metabolism
  • Genetic Fitness
  • Genetic Loci
  • Glucose / pharmacology
  • Haplotypes
  • Intracellular Space / microbiology*
  • Iron / pharmacology
  • Macrophages / drug effects
  • Macrophages / microbiology*
  • Maltose / pharmacology
  • Mice
  • Microbial Viability / drug effects
  • Mutation / genetics
  • Oxidative Stress / drug effects
  • RAW 264.7 Cells

Substances

  • Escherichia coli Proteins
  • Maltose
  • Iron
  • Glucose

Grants and funding

The research leading to these results has received funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007–2013)/ERC grant agreement no 260421 – ECOADAPT. I.G. acknowledges the salary support of LAO/ITQB & FCT.