Effective use of a horizontally-transferred pathway for dichloromethane catabolism requires post-transfer refinement

  1. Joshua K Michener
  2. Aline A Camargo Neves
  3. Stéphane Vuileumier
  4. Françoise Bringel
  5. Christopher J Marx  Is a corresponding author
  1. Harvard University, United States
  2. Harvard University, Cambridge, United States
  3. Université de Strasbourg, France

Abstract

When microbes acquire new abilities through horizontal gene transfer, the genes and pathways must function under conditions with which they did not coevolve. If newly-acquired genes burden the host, effective use will depend on further evolutionary refinement of the recombinant strain. We used laboratory evolution to recapitulate this process of transfer and refinement, demonstrating that effective use of an introduced dichloromethane degradation pathway required one of several mutations to the bacterial host that are predicted to increase chloride efflux. We then used this knowledge to identify parallel, beneficial mutations that independently evolved in two natural dichloromethane-degrading strains. Finally, we constructed a synthetic mobile genetic element carrying both the degradation pathway and a chloride exporter, which preempted the adaptive process and directly enabled effective dichloromethane degradation across diverse Methylobacterium environmental isolates. Our results demonstrate the importance of post-transfer refinement in horizontal gene transfer, with potential applications in bioremediation and synthetic biology.

Article and author information

Author details

  1. Joshua K Michener

    Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Aline A Camargo Neves

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

    Université de Strasbourg, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Françoise Bringel

    Université de Strasbourg, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Christopher J Marx

    Harvard University, Cambridge, United States
    For correspondence
    cmarx@uidaho.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

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

Version history

  1. Received: August 7, 2014
  2. Accepted: November 22, 2014
  3. Accepted Manuscript published: November 24, 2014 (version 1)
  4. Version of Record published: December 22, 2014 (version 2)

Copyright

© 2014, Michener 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. Joshua K Michener
  2. Aline A Camargo Neves
  3. Stéphane Vuileumier
  4. Françoise Bringel
  5. Christopher J Marx
(2014)
Effective use of a horizontally-transferred pathway for dichloromethane catabolism requires post-transfer refinement
eLife 3:e04279.
https://doi.org/10.7554/eLife.04279

Share this article

https://doi.org/10.7554/eLife.04279

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