The birth of a bacterial tRNA gene by large-scale, tandem duplication events

  1. Gökçe B Ayan
  2. Hye Jin Park
  3. Jenna Gallie  Is a corresponding author
  1. Max Planck Institute for Evolutionary Biology, Germany

Abstract

Organisms differ in the types and numbers of tRNA genes that they carry. While the evolutionary mechanisms behind tRNA gene set evolution have been investigated theoretically and computationally, direct observations of tRNA gene set evolution remain rare. Here, we report the evolution of a tRNA gene set in laboratory populations of the bacterium Pseudomonas fluorescens SBW25. The growth defect caused by deleting the single-copy tRNA gene, serCGA, is rapidly compensated by large-scale (45-290 kb) duplications in the chromosome. Each duplication encompasses a second, compensatory tRNA gene (serTGA) and is associated with a rise in tRNA‑Ser(UGA) in the mature tRNA pool. We postulate that tRNA‑Ser(CGA) elimination increases the translational demand for tRNA‑Ser(UGA), a pressure relieved by increasing serTGA copy number. This work demonstrates that tRNA gene sets can evolve through duplication of existing tRNA genes, a phenomenon that may contribute to the presence of multiple, identical tRNA gene copies within genomes.

Data availability

Illumina whole genome sequencing data has been uploaded to NCBI SRA (accession PRJNA558233). YAMAT-seq data has been uploaded to NCBI GEO (accession GSE144791). Source data files have been provided for Figures 2B, 2C, 2D, 2F, 2G, 2H, 3B, 3C, 3D, 3E, 4C, 4D, 5A, and 5B.

The following data sets were generated

Article and author information

Author details

  1. Gökçe B Ayan

    Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Ploen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Hye Jin Park

    Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Ploen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Jenna Gallie

    Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Ploen, Germany
    For correspondence
    gallie@evolbio.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2918-0925

Funding

Max Planck Society

  • Gökçe B Ayan

Max Planck Society

  • Hye Jin Park

Max Planck Society

  • Jenna Gallie

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Vaughn S Cooper, University of Pittsburgh, United States

Publication history

  1. Received: April 16, 2020
  2. Accepted: October 29, 2020
  3. Accepted Manuscript published: October 30, 2020 (version 1)
  4. Version of Record published: November 12, 2020 (version 2)

Copyright

© 2020, Ayan et al.

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. Gökçe B Ayan
  2. Hye Jin Park
  3. Jenna Gallie
(2020)
The birth of a bacterial tRNA gene by large-scale, tandem duplication events
eLife 9:e57947.
https://doi.org/10.7554/eLife.57947

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