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

Elizabeth K Costello,Michael J Morowitz,Erica M Carlisle,David A Relman,Jillian F Banfield,Christine L Sun

doi:10.1038/s41598-017-03821-7

Abstract

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.

Highlights

Mycoplasma species span three clades within the class Mollicutes, a group of obligate parasitic bacteria, affiliated with the phylum Firmicutes, that lack a cell wall
Mycoplasmas are characterized by small cells, small genomes, and metabolic dependence on other organisms—qualities increasingly recognized as widespread across the tree of life[5,6,7]
The taxonomic identities and relative abundances of bacteria were similar to those observed in our earlier survey based on amplified 16S rRNA genes[13] (Supplementary Tables S1, S2 and Fig. S1a)

Summary

Introduction

Mycoplasma species span three clades within the class Mollicutes, a group of obligate parasitic bacteria, affiliated with the phylum Firmicutes, that lack a cell wall They establish relationships as commensals and pathogens of vertebrate hosts; in humans, colonization is typically limited to the mucosal surfaces of the respiratory and urogenital tracts. (lineage ‘Mnola’) that was 85% identical to the closest human-associated species (M. genitalium, M. pneumoniae) and 94% identical to the closest cloned sequences, which are from cattle rumen and termite gut These authors found ‘Mnola’ in 19/30 T. vaginalis-infected and 1/29 uninfected women attending a New Orleans, LA, sexually transmitted infection (STI) clinic[15]. Fettweis et al.[16] detected T. vaginalis in 49/51 women whose vaginal microbiotas comprised at least 1% ‘Mnola’ These authors reported a genome sequence for ‘Mnola’

Methods

Results

Conclusion