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

• DOI: 10.1371/journal.pgen.1004182
• Publication Date: 2014-03-06T21:31:02Z
• Authors: João Barroso-Batista; Ana Sousa; Marta Lourenço; Marie-Louise Bergman; Daniel Sobral; Jocelyne Demengeot; Karina B. Xavier; Isabel Gordo
• Keywords: 0301 basic medicine; QH426-470; Mice; 03 medical and health sciences; Genetics; Escherichia coli; Animals; Humans; Selection, Genetic; Quantitative Biology - Populations and Evolution; Alleles; 0303 health sciences; Models, Genetic; Stomach; Populations and Evolution (q-bio.PE); Genetic Variation; Adaptation, Physiological; 3. Good health; FOS: Biological sciences; Mutation; Cloning; Research Article

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 studied the invasion of beneficial mutations responsible for Escherichia coli's adaptation to the mouse gut and demonstrate the pervasiveness of clonal interference. The observed dynamics of change in frequency of beneficial mutations are consistent with soft sweeps, where a similar adaptive mutation arises repeatedly on different haplotypes without reaching fixation. 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.<br/>46 pages with figures (5 in the main text, 4 in supplementary materials) and tables (7 in supplementary materials). Submitted to PLOS Genetics<br/>