Rapid Genetic Adaptation during the First Four Months of Survival under Resource Exhaustion

Sarit Avrani, Evgeni Bolotin, Sophia Katz, Ruth Hershberg

Research output: Contribution to journalArticlepeer-review

Abstract

Many bacteria, including the model bacterium Escherichia coli can survive for years within spent media, following resource exhaustion. We carried out evolutionary experiments, followed by whole genome sequencing of hundreds of evolved clones to study the dynamics by which E. coli adapts during the first 4 months of survival under resource exhaustion. Our results reveal that bacteria evolving under resource exhaustion are subject to intense selection, manifesting in rapid mutation accumulation, enrichment in functional mutation categories and extremely convergent adaptation. In the most striking example of convergent adaptation, we found that across five independent populations adaptation to conditions of resource exhaustion occurs through mutations to the three same specific positions of the RNA polymerase core enzyme. Mutations to these three sites are strongly antagonistically pleiotropic, in that they sharply reduce exponential growth rates in fresh media. Such antagonistically pleiotropic mutations, combined with the accumulation of additional mutations, severely reduce the ability of bacteria surviving under resource exhaustion to grow exponentially in fresh media. We further demonstrate that the three positions at which these resource exhaustion mutations occur are conserved for the ancestral E. coli allele, across bacterial phyla, with the exception of nonculturable bacteria that carry the resource exhaustion allele at one of these positions, at very high frequencies. Finally, our results demonstrate that adaptation to resource exhaustion is not limited by mutational input and that bacteria are able to rapidly adapt under resource exhaustion in a temporally precise manner through allele frequency fluctuations.

Original languageEnglish
Pages (from-to)1758-1769
Number of pages12
JournalMolecular Biology and Evolution
Volume34
Issue number7
DOIs
StatePublished - 1 Jul 2017

Bibliographical note

Funding Information:
This work was supported by an Ali Kaufman postdoctoral fellowship (to S.A.), by a BSF grant (No. 2013463, to R.H.) by a Yigal Allon Fellowship awarded by the Israeli Council for Higher Education (to R.H.), by the Rappaport Family Institute for Research in the Medical Sciences (to R.H.), and by the Robert J. Shillman Career Advancement Chair (to R.H.). The described research was carried out in the Rachel & Menachem Mendelovitch Evolutionary Process of Mutation & Natural Selection Research Laboratory.

Publisher Copyright:
© The Author 2017.

Keywords

  • Adaptation
  • Antagonistic pleiotropy
  • Convergent evolution
  • Experimental evolution
  • Mutators
  • Resource exhaustion

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

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