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Phylogenetic framework for the phylum Tenericutes based on genome sequence data: proposal for the creation of a new order Mycoplasmoidales ord. nov., containing two new families Mycoplasmoidaceae fam. nov. and Metamycoplasmataceae fam. nov. harbouring Eperythrozoon, Ureaplasma and five novel genera

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A Correction to this article was published on 16 October 2018

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Abstract

The genus Mycoplasma, including species earlier classified in the genera Eperythrozoon and Haemobartonella, contains ~ 120 species and constitutes an extensively polyphyletic assemblage of bacteria within the phylum Tenericutes. Due to their small genome sizes and lack of unique characteristics, the relationships among the mycoplasmas/Tenericutes are not reliably discerned. Using genome sequences for 140 Tenericutes, their evolutionary relationships were examined using multiple independent approaches. Phylogenomic trees were constructed for 63 conserved proteins, 45 ribosomal proteins, three main subunits of RNA polymerase and 16S rRNA gene sequences. In all of these trees, Tenericutes species reliably grouped into four main clades designated as the “Acholeplasma”, “Spiroplasma”, “Pneumoniae” and “Hominis” clusters. These clades are also distinguished based on a similarity matrix constructed based on 16S rRNA gene sequences. Mycoplasma species were dispersed across 3 of these 4 clades highlighting their extensive polyphyly. In parallel, our comparative genomic analyses have identified > 100 conserved signature indels (CSIs) and 14 conserved signature proteins (CSPs), which are uniquely shared by the members of four identified clades, strongly supporting their monophyly and identifying them in molecular terms. Mycoplasma mycoides, the type species of the genus Mycoplasma, and a small number of other Mycoplasma species, formed a strongly supported clade within the “Spiroplasma” cluster. Nine CSIs and 14 CSPs reliably distinguish this clade from all other Mycoplasmatales species. The remainder of the Mycoplasmatales species are part of the “Pneumoniae” and “Hominis” clusters, which group together in phylogenetic trees. Here we are proposing that the order Mycoplasmatales should be emended to encompass only the Mycoplasma species within the “Spiroplasma” cluster and that a new order, Mycoplasmoidales ord. nov., should be created to encompass the other Mycoplasma species. The “Pneumoniae” and the “Hominis” clusters are proposed as two new families, Mycoplasmoidaceae fam. nov., which includes the genera Eperythrozoon, Ureaplasma, and the newly proposed genera Malacoplasma and Mycoplasmoides, and Metamycoplasmataceae fam. nov. to contain the newly proposed genera Metamycoplasma, Mycoplasmopsis, and Mesomycoplasma. The results presented here allow reliable discernment, both in phylogenetic and molecular terms, of the members of the two proposed families as well as different described genera within these families including members of the genus Eperythrozoon, which is comprised of uncultivable organisms. The taxonomic reclassifications proposed here, which more accurately portray the genetic diversity among the Tenericutes/Mycoplasma species, provide a new framework for understanding the biological and clinical aspects of these important microbes.

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Change history

  • 16 October 2018

    In Tables 9, 10 and 11 of this paper, a few minor errors were noticed in the information for the type strains of the following new name combinations proposed in our paper.

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Acknowledgements

We thank Judy Tran, Talha Tahir, Jeen Son and Joseph Manalo for assistance in the identification and formatting of some of the described CSIs and CSPs. We also thank the editor Dr. Iain Sutcliffe for many helpful suggestions concerning the work presented here. This work was supported by Research Grant No. 249924 from the Natural Science and Engineering Research Council of Canada awarded to Radhey S. Gupta.

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Authors and Affiliations

  1. Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, ON, L8N 3Z5, Canada

    Radhey S. Gupta, Sahil Sawnani, Mobolaji Adeolu & Seema Alnajar

  2. Department of Plant and Environmental Sciences, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, The Edmond J. Safra Campus, 9190401, Jerusalem, Israel

    Aharon Oren

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  1. Radhey S. Gupta
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  2. Sahil Sawnani
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Correspondence to Radhey S. Gupta.

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Gupta, R.S., Sawnani, S., Adeolu, M. et al. Phylogenetic framework for the phylum Tenericutes based on genome sequence data: proposal for the creation of a new order Mycoplasmoidales ord. nov., containing two new families Mycoplasmoidaceae fam. nov. and Metamycoplasmataceae fam. nov. harbouring Eperythrozoon, Ureaplasma and five novel genera. Antonie van Leeuwenhoek 111, 1583–1630 (2018). https://doi.org/10.1007/s10482-018-1047-3

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