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Front. Microbiol. | doi: 10.3389/fmicb.2018.02493

Evolutionary History of Copper Membrane Monooxygenases

  • 1Department of Biological Sciences, University of Calgary, Canada
  • 2Georgia State University, United States
  • 3City University of Hong Kong, Hong Kong
  • 4Washington State University Tri-Cities, United States

Copper membrane monooxygenases (CuMMOs) oxidize ammonia, methane and some short-chain alkanes and alkenes. They are encoded by three genes, usually in an operon of xmoCAB. We aligned xmo operons from 66 microbial genomes, including members of the Alpha-, Beta-, and Gammaproteobacteria, Verrucomicrobia, Actinobacteria, Thaumarchaeota and the candidate phylum NC10. Phylogenetic and compositional analyses were used to reconstruct the evolutionary history of the enzyme and detect potential lateral gene transfer (LGT) events. The phylogenetic analyses showed at least 10 clusters corresponding to a combination of substrate specificity and bacterial taxonomy, but with no overriding structuring based on either function or taxonomy alone. Adaptation of the enzyme to preferentially oxidise either ammonia or methane has occurred more than once. Individual phylogenies of all three genes, xmoA, xmoB and xmoC, closely matched, indicating that this operon evolved or was consistently transferred as a unit, with the possible exception of the methane monooxygenase operons in Verrucomicrobia, where the pmoB gene has a distinct phylogeny from pmoA and pmoC. Compositional analyses indicated that some clusters of xmoCAB operons (for example, the pmoCAB in gammaproteobacterial methanotrophs and the amoCAB in betaproteobacterial nitrifiers) were compositionally very different from their genomes, possibly indicating recent lateral transfer of these operons. The combined phylogenetic and compositional analyses support the hypothesis that an ancestor of the nitrifying bacterium Nitrosococcus was the donor of methane monooxygenase (pMMO) to both the alphaproteobacterial and gammaproteobacterial methanotrophs, but that before this event the gammaproteobacterial methanotrophs originally possessed another CuMMO (Pxm), which has since been lost in many species.

Keywords: Methane oxidation, ammonia oxidation, copper membrane monooxygenase, Lateral gene transfer, phylogenetics

Received: 27 Jun 2018; Accepted: 28 Sep 2018.

Edited by:

Frank T. Robb, University of Maryland, Baltimore, United States

Reviewed by:

Susannah G. Tringe, Joint Genome Institute (JGI), United States
Nils-Kaare Birkeland, University of Bergen, Norway
Sukhwan Yoon, Korea Advanced Institute of Science & Technology (KAIST), South Korea  

Copyright: © 2018 KHADKA, Clothier, Wang, Lim, Klotz and Dunfield. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Peter Dunfield, Department of Biological Sciences, University of Calgary, Calgary, Canada,