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A mutational hotspot that determines highly repeatable evolution can be built and broken by silent genetic changes

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  • James S. Horton

    (University of Bath, Claverton Down)

  • Louise M. Flanagan

    (University of Bath, Claverton Down)

  • Robert W. Jackson

    (University of Birmingham, Edgbaston)

  • Nicholas K. Priest

    (University of Bath, Claverton Down)

  • Tiffany B. Taylor

    (University of Bath, Claverton Down)

Abstract

Mutational hotspots can determine evolutionary outcomes and make evolution repeatable. Hotspots are products of multiple evolutionary forces including mutation rate heterogeneity, but this variable is often hard to identify. In this work, we reveal that a near-deterministic genetic hotspot can be built and broken by a handful of silent mutations. We observe this when studying homologous immotile variants of the bacteria Pseudomonas fluorescens, AR2 and Pf0-2x. AR2 resurrects motility through highly repeatable de novo mutation of the same nucleotide in >95% lines in minimal media (ntrB A289C). Pf0-2x, however, evolves via a number of mutations meaning the two strains diverge significantly during adaptation. We determine that this evolutionary disparity is owed to just 6 synonymous variations within the ntrB locus, which we demonstrate by swapping the sites and observing that we are able to both break (>95% to 0%) and build (0% to 80%) a deterministic mutational hotspot. Our work reveals a key role for silent genetic variation in determining adaptive outcomes.

Suggested Citation

  • James S. Horton & Louise M. Flanagan & Robert W. Jackson & Nicholas K. Priest & Tiffany B. Taylor, 2021. "A mutational hotspot that determines highly repeatable evolution can be built and broken by silent genetic changes," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26286-9
    DOI: 10.1038/s41467-021-26286-9
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    References listed on IDEAS

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    1. Zachary D. Blount & Jeffrey E. Barrick & Carla J. Davidson & Richard E. Lenski, 2012. "Genomic analysis of a key innovation in an experimental Escherichia coli population," Nature, Nature, vol. 489(7417), pages 513-518, September.
    2. Patrick T. McGrath & Yifan Xu & Michael Ailion & Jennifer L. Garrison & Rebecca A. Butcher & Cornelia I. Bargmann, 2011. "Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes," Nature, Nature, vol. 477(7364), pages 321-325, September.
    3. Christopher N. Merrikh & Houra Merrikh, 2018. "Gene inversion potentiates bacterial evolvability and virulence," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
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    Cited by:

    1. Noor Radde & Genevieve A. Mortensen & Diya Bhat & Shireen Shah & Joseph J. Clements & Sean P. Leonard & Matthew J. McGuffie & Dennis M. Mishler & Jeffrey E. Barrick, 2024. "Measuring the burden of hundreds of BioBricks defines an evolutionary limit on constructability in synthetic biology," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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