Skip to main content
bioRxiv
  • Home
  • About
  • Submit
  • ALERTS / RSS
Advanced Search
New Results

Extreme parallel evolution of flagellar motility facilitated by silent mutations

View ORCID ProfileJames S. Horton, Louise M. Flanagan, Robert W. Jackson, View ORCID ProfileNicholas K. Priest, View ORCID ProfileTiffany B. Taylor
doi: https://doi.org/10.1101/2021.01.04.425178
James S. Horton
1Milner Centre for Evolution, Department of Biology & Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for James S. Horton
  • For correspondence: j.s.horton@bath.ac.uk t.b.taylor@bath.ac.uk
Louise M. Flanagan
1Milner Centre for Evolution, Department of Biology & Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert W. Jackson
2School of Biosciences and Birmingham Institute of Forest Research (BIFoR), University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nicholas K. Priest
1Milner Centre for Evolution, Department of Biology & Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Nicholas K. Priest
Tiffany B. Taylor
1Milner Centre for Evolution, Department of Biology & Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Tiffany B. Taylor
  • For correspondence: j.s.horton@bath.ac.uk t.b.taylor@bath.ac.uk
  • Abstract
  • Full Text
  • Info/History
  • Metrics
  • Data/Code
  • Preview PDF
Loading

Abstract

There is a growing need for accurate evolutionary forecasting, but we must first understand how possible evolutionary paths can be constrained by silent genetic features. Here we show that synonymous sequence variation determines extreme parallel evolution during the evolutionary rescue of flagellar motility. An immotile variant of the soil microbe, Pseudomonas fluorescens, swiftly recovers flagellum-dependent motility through parallel de novo mutation. This typically manifests within 96 h under strong selection through repeatable mutation within the nitrogen pathway’s histidine kinase gene, ntrB. We found that evolution was parallel to nucleotide resolution in over 95% of cases in minimal medium (M9), with lineages repeatedly fixing an identical mutation (ntrB A289C). There was no evidence that this substitution is context-specific, as repeatable de novo mutation was robust to nutrient condition despite evidence for antagonistic pleiotropy. Competition assays against alternative motile alleles revealed some evidence for selection enforcing repeated fixation of ntrB mutants, but there was no evidence for clonal interference driving parallel evolution to nucleotide resolution. Instead, the introduction of 6 synonymous substitutions surrounding the mutational hotspot reduced parallel evolution from >95% to 0% at the site. In a reciprocal experiment, we introduced 6 synonymous substitutions into a homologous strain that did not ancestrally evolve in parallel and observed that parallel evolution at the site rose from 0% to 80%. We propose that these silent mutations facilitate extremely localised heterogeneity in de novo mutation. Our results reveal that unique quirks in how DNA is structured at specific loci can strongly bias evolutionary outcomes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵a These authors share senior authorship

  • The manuscript now includes figure 5; the abstract, results and discussion sections have been updated to incorporate this new data; the author list has been updated.

  • https://github.com/J-S-Horton/Syn-sequence-parallel-evolution.git

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
Back to top
PreviousNext
Posted January 11, 2021.
Download PDF
Data/Code
Email

Thank you for your interest in spreading the word about bioRxiv.

NOTE: Your email address is requested solely to identify you as the sender of this article.

Enter multiple addresses on separate lines or separate them with commas.
Extreme parallel evolution of flagellar motility facilitated by silent mutations
(Your Name) has forwarded a page to you from bioRxiv
(Your Name) thought you would like to see this page from the bioRxiv website.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Extreme parallel evolution of flagellar motility facilitated by silent mutations
James S. Horton, Louise M. Flanagan, Robert W. Jackson, Nicholas K. Priest, Tiffany B. Taylor
bioRxiv 2021.01.04.425178; doi: https://doi.org/10.1101/2021.01.04.425178
Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Extreme parallel evolution of flagellar motility facilitated by silent mutations
James S. Horton, Louise M. Flanagan, Robert W. Jackson, Nicholas K. Priest, Tiffany B. Taylor
bioRxiv 2021.01.04.425178; doi: https://doi.org/10.1101/2021.01.04.425178

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Subject Area

  • Evolutionary Biology
Subject Areas
All Articles
  • Animal Behavior and Cognition (2513)
  • Biochemistry (4957)
  • Bioengineering (3456)
  • Bioinformatics (15148)
  • Biophysics (6868)
  • Cancer Biology (5365)
  • Cell Biology (7692)
  • Clinical Trials (138)
  • Developmental Biology (4509)
  • Ecology (7117)
  • Epidemiology (2059)
  • Evolutionary Biology (10193)
  • Genetics (7494)
  • Genomics (9758)
  • Immunology (4808)
  • Microbiology (13153)
  • Molecular Biology (5114)
  • Neuroscience (29321)
  • Paleontology (203)
  • Pathology (833)
  • Pharmacology and Toxicology (1458)
  • Physiology (2123)
  • Plant Biology (4723)
  • Scientific Communication and Education (1004)
  • Synthetic Biology (1336)
  • Systems Biology (3997)
  • Zoology (768)