Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.

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...

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Main Authors: Antonella Marangoni, Camilla Ceccarani, Tania Camboni, Clarissa Consolandi, Claudio Foschi, Melissa Salvo, Valeria Gaspari, Antonietta D'Antuono, Matteo Belletti, Maria Carla Re, Marco Severgnini
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0227985
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spelling doaj-3afe1b9276104ef9bc63529e81f57ce12021-03-03T21:31:40ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01151e022798510.1371/journal.pone.0227985Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.Antonella MarangoniCamilla CeccaraniTania CamboniClarissa ConsolandiClaudio FoschiMelissa SalvoValeria GaspariAntonietta D'AntuonoMatteo BellettiMaria Carla ReMarco SevergniniPharyngeal 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 NG-infected 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.https://doi.org/10.1371/journal.pone.0227985
collection DOAJ
language English
format Article
sources DOAJ
author Antonella Marangoni
Camilla Ceccarani
Tania Camboni
Clarissa Consolandi
Claudio Foschi
Melissa Salvo
Valeria Gaspari
Antonietta D'Antuono
Matteo Belletti
Maria Carla Re
Marco Severgnini
spellingShingle Antonella Marangoni
Camilla Ceccarani
Tania Camboni
Clarissa Consolandi
Claudio Foschi
Melissa Salvo
Valeria Gaspari
Antonietta D'Antuono
Matteo Belletti
Maria Carla Re
Marco Severgnini
Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.
PLoS ONE
author_facet Antonella Marangoni
Camilla Ceccarani
Tania Camboni
Clarissa Consolandi
Claudio Foschi
Melissa Salvo
Valeria Gaspari
Antonietta D'Antuono
Matteo Belletti
Maria Carla Re
Marco Severgnini
author_sort Antonella Marangoni
title Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.
title_short Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.
title_full Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.
title_fullStr Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.
title_full_unstemmed Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection.
title_sort pharyngeal microbiome alterations during neisseria gonorrhoeae infection.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description 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 NG-infected 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.
url https://doi.org/10.1371/journal.pone.0227985
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