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Front. Microbiol. | doi: 10.3389/fmicb.2018.03162

Phylogenomic Analysis of the Gammaproteobacterial Methanotrophs (Order Methylococcales) Calls for the Reclassification of Members at the Genus and Species Levels

  • 1Department of Chemical and Materials Engineering, Faculty of Engineering, University of Alberta, Canada
  • 2Department of Biological Sciences, Faculty of Science, University of Alberta, Canada
  • 3Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ), Germany

The order Methylococcales constitutes the methanotrophs – bacteria that can metabolize methane, a potent greenhouse gas, as their sole source of energy. These bacteria are significant players in the global carbon cycle and can produce value-added products from methane, such as biopolymers, biofuels, and single-cell proteins for animal feed, among others. Previous studies using single-gene phylogenies have shown inconsistencies in the currently established taxonomic structure of this group. This study aimed to determine and resolve these issues by using whole-genome sequence analyses. Phylogenomic analysis and the use of similarity indexes for genomic comparisons – average amino acid identity (AAI), digital DNA–DNA hybridization (dDDH), and average nucleotide identity (ANI) – were performed on 91 Methylococcales genomes. Results suggest the reclassification of members at the genus and species levels. Firstly, to resolve polyphyly of the genus Methylomicrobium, Methylomicrobium alcaliphilum, “Methylomicrobium buryatense”, Methylomicrobium japanense, Methylomicrobium kenyense, and Methylomicrobium pelagicum are reclassified to a newly proposed genus, Methylotuvimicrobium gen. nov.; they are therefore renamed to Methylotuvimicrobium alcaliphilum comb. nov., “Methylotuvimicrobium buryatense” comb. nov., Methylotuvimicrobium japanense comb. nov., Methylotuvimicrobium kenyense comb. nov., and Methylotuvimicrobium pelagicum comb. nov., respectively. Secondly, due to the phylogenetic affinity and phenotypic similarities of Methylosarcina lacus with Methylomicrobium agile and Methylomicrobium album, the reclassification of the former species to Methylomicrobium lacus comb. nov. is proposed. Thirdly, using established same-species delineation thresholds (70% dDDH and 95% ANI), Methylobacter whittenburyi is proposed to be a later heterotypic synonym of Methylobacter marinus (89% dDDH and 99% ANI). Also, the effectively but not validly published “Methylomonas denitrificans” was identified as Methylomonas methanica (92% dDDH and 100% ANI), indicating that the former is a later heterotypic synonym of the latter. Lastly, strains MC09, R-45363, and R-45371, currently identified as M. methanica, each represent a putative novel species of the genus Methylomonas (21–35% dDDH and 74–88% ANI against M. methanica) and were reclassified as Methylomonas sp. strains. It is imperative to resolve taxonomic inconsistencies within this group, first and foremost, to avoid confusion with ecological and evolutionary interpretations in subsequent studies.

Keywords: Gammaproteobacteria, Methylococcales, methanotroph, Methylotuvimicrobium gen. nov., Genome-based taxonomy, whole-genome phylogeny, Genome BLAST Distance Phylogeny, digital DNA–DNA hybridization, Average nucleotide identity, Average amino acid identity

Received: 05 Oct 2018; Accepted: 06 Dec 2018.

Edited by:

Iain Sutcliffe, Northumbria University, United Kingdom

Reviewed by:

Claudia Knief, Universität Bonn, Germany
Svetlana N. Dedysh, Winogradsky Institute of Microbiology (RAS), Russia  

Copyright: © 2018 Orata, Meier-Kolthoff, Sauvageau and Stein. 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: Dr. Fabini D. Orata, Department of Chemical and Materials Engineering, Faculty of Engineering, University of Alberta, Edmonton, T6G 1H9, Alberta, Canada, fabini.orata@gmail.com