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Systematic bacterialization of yeast genes identifies a near-universally swappable pathway

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Cite this article as: eLife 2017;6:e25093 doi: 10.7554/eLife.25093

Abstract

Eukaryotes and prokaryotes last shared a common ancestor ~2 billion years ago, and while many present-day genes in these lineages predate this divergence, the extent to which these genes still perform their ancestral functions is largely unknown. To test principles governing retention of ancient function, we asked if prokaryotic genes could replace their essential eukaryotic orthologs. We systematically replaced essential genes in yeast by their 1:1 orthologs from Escherichia coli. After accounting for mitochondrial localization and alternative start codons, 31 out of 51 bacterial genes tested (61%) could complement a lethal growth defect and replace their yeast orthologs with minimal effects on growth rate. Replaceability was determined on a pathway-by-pathway basis; codon usage, abundance, and sequence similarity contributed predictive power. The heme biosynthesis pathway was particularly amenable to inter-kingdom exchange, with each yeast enzyme replaceable by its bacterial, human, or plant ortholog, suggesting it as a near-universally swappable pathway.

Article and author information

Author details

  1. Aashiq Hussain Kachroo

    Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, United States
    For correspondence
    aashiq@utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9770-778X
  2. Jon Michael Laurent

    Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6583-4741
  3. Azat Akhmetov

    Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Madelyn Szilagyi-Jones

    Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Claire Darnell McWhite

    Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alice Zhao

    Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Edward Michael Marcotte

    Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, United States
    For correspondence
    marcotte@icmb.utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8808-180X

Funding

National Institutes of Health

  • Edward Michael Marcotte

Cancer Prevention and Research Institute of Texas

  • Edward Michael Marcotte

Welch Foundation (F1515)

  • Edward Michael Marcotte

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

Reviewing Editor

  1. Naama Barkai, Weizmann Institute of Science, Israel

Publication history

  1. Received: January 12, 2017
  2. Accepted: June 26, 2017
  3. Accepted Manuscript published: June 29, 2017 (version 1)
  4. Accepted Manuscript updated: June 30, 2017 (version 2)
  5. Version of Record published: July 31, 2017 (version 3)
  6. Version of Record updated: August 4, 2017 (version 4)
  7. Version of Record updated: April 6, 2018 (version 5)

Copyright

© 2017, Kachroo 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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