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Genital mycoplasmas, which can be vertically transmitted, have been implicated in preterm birth, neonatal infections, and chronic lung disease of prematurity. Our prior work uncovered 16S rRNA genes belonging to a novel, as-yet-uncultivated mycoplasma (lineage ‘Mnola’) in the oral cavity of a premature neonate. Here, we characterize the organism’s associated community, growth status, metabolic potential, and population diversity. Sequencing of genomic DNA from the infant’s saliva yielded 1.44 Gbp of high-quality, non-human read data, from which we recovered three essentially complete (including ‘Mnola’) and three partial draft genomes (including  Trichomonas vaginalis ). The completed 629,409-bp ‘Mnola’ genome ( Candidatus  Mycoplasma girerdii str. UC-B3) was distinct at the strain level from its closest relative, vaginally-derived  Ca . M. girerdii str. VCU-M1, which is also associated with  T .  vaginalis . Replication rate measurements indicated growth of str. UC-B3 within the infant. Genes encoding surface-associated proteins and restriction-modification systems were especially diverse within and between strains. In UC-B3, the population genetic underpinnings of phase variable expression were evident  in vivo . Unique among mycoplasmas,  Ca . M. girerdii encodes pyruvate-ferredoxin oxidoreductase and may be sensitive to metronidazole. This study reveals a metabolically unique mycoplasma colonizing a premature neonate, and establishes the value of genome-resolved metagenomics in tracking phase variation.

Candidatus Mycoplasma girerdii replicates, diversifies, and co-occurs with Trichomonas vaginalis in the oral cavity of a premature infant