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Antonie van Leeuwenhoek

, Volume 111, Issue 9, pp 1583–1630 | Cite as

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

  • Radhey S. Gupta
  • Sahil Sawnani
  • Mobolaji Adeolu
  • Seema Alnajar
  • Aharon Oren
Original Paper

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.

Keywords

Tenericutes Order Mycoplasmatales Mycoplasma Eperythrozoon Haemobartonella Phylogeny Taxonomy Conserved signature indels Phylogenomic studies Comparative genomics Molecular signatures 

Notes

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.

Conflict of interest

All of the authors declare that they have no conflict of interest.

Supplementary material

10482_2018_1047_MOESM1_ESM.pdf (3 mb)
Supplementary material 1 (PDF 3107 kb)

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Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Radhey S. Gupta
    • 1
  • Sahil Sawnani
    • 1
  • Mobolaji Adeolu
    • 1
  • Seema Alnajar
    • 1
  • Aharon Oren
    • 2
  1. 1.Department of Biochemistry and Biomedical SciencesMcMaster UniversityHamiltonCanada
  2. 2.Department of Plant and Environmental Sciences, The Alexander Silberman Institute of Life SciencesThe Hebrew University of JerusalemJerusalemIsrael

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