Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection

Abstract

Pharyngeal gonorrhoea is a common sexually transmitted infection among 'men having sex with other men' (MSM). Neisseria gonorrhoeae (NG) pharyngeal infections are usually characterized by the absence of symptoms, acting as an important reservoir for their further spread. To the best of our knowledge, no information about the composition of the pharyngeal microbiome during an ongoing NG infection is currently available. Therefore, in this study, we characterized the pharyngeal bacterial community profiles associated with NG infection in a well-selected cohort of HIV-negative MSM reporting unsafe oral intercourse. A total of 70 pharyngeal swabs were considered, comparing non-infected subjects (n = 45) versus patients with pharyngeal gonorrhoea (n = 25) whose microbiota composition was analyzed from pharyngeal swabs through sequencing of hypervariable V3-V4 regions of the 16S rRNA gene. The pharyngeal microbiome of all subjects was dominated by Prevotellaceae, Veillonellaceae and Streptococcaceae families. Patients with pharyngeal gonorrhoea harboured a pharyngeal microbiome quite similar to negative subjects. Nevertheless, when looking to less-represented bacterial species (relative abundance approximately 1% or less), an imbalance between aerobe and anaerobe microorganisms was observed in NGinfected patients. In particular, the pharyngeal microbiome of NG-positive individuals was richer in several anaerobes (e.g. Treponema, Parvimonas, Peptococcus, Catonella, Filifactor) and poorer in various aerobe genera (i.e. Pseudomonas, Escherichia), compared to non-infected controls. No significant differences were noticed in the distribution of commensal Neisseria species of the oropharynx between NG-positive and negative subjects. Metabolic variations induced by changes in the microbiome abundance were assessed by a functional prediction of the bacterial metabolic pathways: a more abundant involvement of D-glutamine and D-glutamate metabolism, carbohydrate metabolism, as well as a greater activation of the energy metabolism was observed in patients with pharyngeal gonorrhoea compared to non-infected individuals. Information about the bacterial composition of the pharyngeal microbiome in case of gonorrhoea could shed light on the pathogenesis of the infection and open new perspectives for the prevention and control of this condition.

The Impact of Mouthwash on the Oropharyngeal Microbiota of Men Who Have Sex with Men: a Substudy of the OMEGA Trial

“…Consistent with our findings, Marangoni et al ( 42 ) reported no differences in the overall structure of the oropharyngeal microbiota in infected versus noninfected men. However, in contrast to our findings, Marangoni et al ( 42 ) found that infected men had an increased abundance of anaerobic bacteria (including Treponema , Parvimonas , and Peptococcus ) and a decreased abundance of aerobic bacteria (including Pseudomonas and Escherichia ). Although the differences between the two studies could be a result of population differences, they could also have resulted from differences in statistical method applied.…”

“…This is perhaps surprising, as N. gonorrhoeae infection has been associated with alterations in the composition of the rectal microbiome ( 41 ). Only one other study has described the oral microbiota composition in individuals with oropharyngeal gonorrhea ( 42 ). Consistent with our findings, Marangoni et al ( 42 ) reported no differences in the overall structure of the oropharyngeal microbiota in infected versus noninfected men.…”

“…Only one other study has described the oral microbiota composition in individuals with oropharyngeal gonorrhea ( 42 ). Consistent with our findings, Marangoni et al ( 42 ) reported no differences in the overall structure of the oropharyngeal microbiota in infected versus noninfected men. However, in contrast to our findings, Marangoni et al ( 42 ) found that infected men had an increased abundance of anaerobic bacteria (including Treponema , Parvimonas , and Peptococcus ) and a decreased abundance of aerobic bacteria (including Pseudomonas and Escherichia ).…”

“…To our knowledge, Marangoni et al ( 42 ) present the only other analysis of the oral microbiota composition of MSM. We found the composition of the oropharyngeal microbiota of MSM to be very similar to that reported by Marangoni et al ( 42 ), with Prevotella , Veillonella , Fusobacterium , and Streptococcus representing the most abundant genera in both studies.…”

Meningococcal Carriage in ‘Men Having Sex With Men’ With Pharyngeal Gonorrhoea

“…From what has been said so far, it is evident that both NM and GC can be found in the oro-pharynx, that represents a suitable ecological niche for Neisseria species to replicate and persist over time ( Marangoni et al., 2020a ).…”