Evolving a 24-hour oscillator in budding yeast

  1. Gregg A Wildenberg  Is a corresponding author
  2. Andrew W Murray
  1. Harvard University, United States

Abstract

We asked how a new, complex trait evolves by selecting for diurnal oscillations in the budding yeast, Saccharomyces cerevisiae. We expressed yellow fluorescent protein (YFP) from a yeast promoter and selected for a regular alternation between low and high fluorescence over 24-hour period. This selection produced changes in cell adhesion rather than YFP expression: clonal populations oscillated between single cells and multicellular clumps. The oscillations are not a response to environmental cues and continue for at least three cycles in a constant environment. We identified eight putative causative mutations in one clone and recreated the evolved phenotype in the ancestral strain. The mutated genes lack obvious relationships to each other, but multiple lineages change from the haploid to the diploid pattern of gene expression. We show that a novel, complex phenotype can evolve by small sets of mutations in genes whose molecular functions appear to be unrelated to each other.

Article and author information

Author details

  1. Gregg A Wildenberg

    Harvard University, Cambridge, United States
    For correspondence
    greggwildenberg@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Andrew W Murray

    Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Michael Laub, Massachusetts Institute of Technology, United States

Publication history

  1. Received: September 23, 2014
  2. Accepted: November 7, 2014
  3. Accepted Manuscript published: November 10, 2014 (version 1)
  4. Version of Record published: December 10, 2014 (version 2)

Copyright

© 2014, Wildenberg & Murray

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Gregg A Wildenberg
  2. Andrew W Murray
(2014)
Evolving a 24-hour oscillator in budding yeast
eLife 3:e04875.
https://doi.org/10.7554/eLife.04875

Further reading

    1. Evolutionary Biology
    2. Microbiology and Infectious Disease
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    Bacterial pathogens show high levels of chromosomal genetic diversity, but the influence of this diversity on the evolution of antibiotic resistance by plasmid acquisition remains unclear. Here, we address this problem in the context of colistin, a ‘last line of defence’ antibiotic. Using experimental evolution, we show that a plasmid carrying the MCR-1 colistin resistance gene dramatically increases the ability of Escherichia coli to evolve high-level colistin resistance by acquiring mutations in lpxC, an essential chromosomal gene involved in lipopolysaccharide biosynthesis. Crucially, lpxC mutations increase colistin resistance in the presence of the MCR-1 gene, but decrease the resistance of wild-type cells, revealing positive sign epistasis for antibiotic resistance between the chromosomal mutations and a mobile resistance gene. Analysis of public genomic datasets shows that lpxC polymorphisms are common in pathogenic E. coli, including those carrying MCR-1, highlighting the clinical relevance of this interaction. Importantly, lpxC diversity is high in pathogenic E. coli from regions with no history of MCR-1 acquisition, suggesting that pre-existing lpxC polymorphisms potentiated the evolution of high-level colistin resistance by MCR-1 acquisition. More broadly, these findings highlight the importance of standing genetic variation and plasmid/chromosomal interactions in the evolutionary dynamics of antibiotic resistance.