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

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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.

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Joshua K Michener

Harvard University, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.
Aline A Camargo Neves

Harvard University, Cambridge, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.
Stéphane Vuileumier

Université de Strasbourg, Strasbourg, France

Competing interests
The authors declare that no competing interests exist.
Françoise Bringel

Université de Strasbourg, Strasbourg, France

Competing interests
The authors declare that no competing interests exist.
Christopher J Marx

Harvard University, Cambridge, United States

For correspondence
cmarx@uidaho.edu

Competing interests
The authors declare that no competing interests exist.

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