The First Steps of Adaptation of Escherichia coli to the Gut Are Dominated by Soft Sweeps

João Barroso-Batista,Marie-Louise Bergman,Jocelyne Demengeot,Daniel Sobral,Ana Sousa,Marta Lourenço,Isabel Gordo,Karina B Xavier,Graham Coop

doi:10.1371/journal.pgen.1004182

João Barroso-Batista, Marie-Louise Bergman + Show 7 more

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https://doi.org/10.1371/journal.pgen.1004182

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Abstract

The accumulation of adaptive mutations is essential for survival in novel environments. However, in clonal populations with a high mutational supply, the power of natural selection is expected to be limited. This is due to clonal interference - the competition of clones carrying different beneficial mutations - which leads to the loss of many small effect mutations and fixation of large effect ones. If interference is abundant, then mechanisms for horizontal transfer of genes, which allow the immediate combination of beneficial alleles in a single background, are expected to evolve. However, the relevance of interference in natural complex environments, such as the gut, is poorly known. To address this issue, we have developed an experimental system which allows to uncover the nature of the adaptive process as Escherichia coli adapts to the mouse gut. This system shows the invasion of beneficial mutations in the bacterial populations and demonstrates the pervasiveness of clonal interference. The observed dynamics of change in frequency of beneficial mutations are consistent with soft sweeps, where different adaptive mutations with similar phenotypes, arise repeatedly on different haplotypes without reaching fixation. Despite the complexity of this ecosystem, the genetic basis of the adaptive mutations revealed a striking parallelism in independently evolving populations. This was mainly characterized by the insertion of transposable elements in both coding and regulatory regions of a few genes. Interestingly, in most populations we observed a complete phenotypic sweep without loss of genetic variation. The intense clonal interference during adaptation to the gut environment, here demonstrated, may be important for our understanding of the levels of strain diversity of E. coli inhabiting the human gut microbiota and of its recombination rate.

Highlights

Mutation is the fuel of evolution and beneficial mutations the driver of organismal adaptation
We show that clonal interference is pervasive in the mouse gut and that the targets of natural selection are similar in independently E. coli evolving populations
Stable marker dynamics are expected under two completely opposing scenarios: neutral evolution due to the lack of occurrence of adaptive mutations, or very intense clonal interference (CI) caused by strong mutations of similar effect occurring in the different fluorescence backgrounds simultaneously

Summary

Introduction

Mutation is the fuel of evolution and beneficial mutations the driver of organismal adaptation. If the rate of emergence of new beneficial mutations is low, adaptation will proceed through the asynchronous accumulation of such mutations, one at a time. This will result in short-term polymorphism, during which the frequency of the beneficial mutation will rapidly change. Such strong selective sweeps will purge linked neutral variation, a phenomenon long recognized as the signature of selective sweeps in bacterial populations [1]. For reasonably small populations and for low mutation rates, population mean fitness will increase in steps, where at each step neutral variation becomes completely depleted. The adaptive walk will proceed by discrete movements along the fitness landscape

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