Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection
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Antonella Marangoni aff001; Camilla Ceccarani aff002; Tania Camboni aff002; Clarissa Consolandi aff002; Claudio Foschi aff001; Melissa Salvo aff001; Valeria Gaspari aff004; Antonietta D’Antuono aff004; Matteo Belletti aff004; Maria Carla Re aff001; Marco Severgnini aff002
Působiště autorů:
Microbiology, DIMES, University of Bologna, Bologna, Italy
aff001; Institute of Biomedical Technologies–National Research Council, Segrate, Milan, Italy
aff002; Department of Health Sciences, University of Milan, Milan, Italy
aff003; Dermatology, St. Orsola-Malpighi Hospital, Bologna, Italy
aff004
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0227985
Souhrn
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.
Klíčová slova:
Anaerobic bacteria – Carbohydrate metabolism – Microbiome – Neisseria – Neisseria gonorrhoeae – Oropharynx – Sexually transmitted diseases – Xenobiotic metabolism
Zdroje
1. Gaspari V, Marangoni A, D'Antuono A, Roncarati G, Salvo M, Foschi C, et al. Pharyngeal Chlamydia and gonorrhea: a hidden problem. Int J STD AIDS. 2019;2: 956462419838922.
2. Patton ME, Kidd S, Llata E, Stenger M, Braxton J, Asbel L, et al. Extragenital gonorrhea and chlamydia testing and infection among men who have sex with men—STD Surveillance Network, United States, 2010–2012. Clin Infect Dis. 2014;58: 1564–1570. doi: 10.1093/cid/ciu184 24647015
3. Chan PA, Robinette A, Montgomery M, Almonte A, Cu-Uvin S, Lonks JR, et al. Extragenital Infections Caused by Chlamydia trachomatis and Neisseria gonorrhoeae: A Review of the Literature. Infect Dis Obstet Gynecol. 2016;2016: 5758387. doi: 10.1155/2016/5758387 27366021
4. Reinton N, Moi H, Olsen AO, Zarabyan N, Bjerner J, Tønseth TM, et al. Anatomic distribution of Neisseria gonorrhoeae, Chlamydia trachomatis and Mycoplasma genitalium infections in men who have sex with men. Sex Health. 2013;10: 199–203. doi: 10.1071/SH12092 23751932
5. Regan DG, Hui BB, Wood JG, Fifer H, Lahra MM, Whiley DM. Treatment for pharyngeal gonorrhoea under threat. Lancet Infect Dis. 2018;18: 1175–1177. doi: 10.1016/S1473-3099(18)30610-8 30507396
6. Quillin SJ and Seifert HS. Neisseria gonorrhoeae host adaptation and pathogenesis. Nat Rev Microbiol 2018; 16(4): 226–240. doi: 10.1038/nrmicro.2017.169 29430011
7. Dong HV, Pham LQ, Nguyen HT, Nguyen MXB, Nguyen TV, May F, et al. Decreased Cephalosporin Susceptibility of Oropharyngeal Neisseria Species in Antibiotic-Using Men-who-have-sex-with-men of Hanoi, Vietnam. Clin Infect Dis. 2019:pii: ciz365. doi: 10.1093/cid/ciz365 31049592
8. Unemo M, Shafer WM. Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin Microbiol Rev. 2014;27: 587–613. doi: 10.1128/CMR.00010-14 24982323
9. Chow EPF, Walker S, Read TRH, Chen MY, Bradshaw CS, Fairley CK. Self-Reported Use of Mouthwash and Pharyngeal Gonorrhoea Detection by Nucleic Acid Amplification Test. Sex Transm Dis. 2017;44: 593–595. doi: 10.1097/OLQ.0000000000000654 28876323
10. Walker S, Bellhouse C, Fairley CK, Bilardi JE, Chow EP. Pharyngeal Gonorrhoea: The Willingness of Australian Men Who Have Sex with Men to Change Current Sexual Practices to Reduce Their Risk of Transmission-A Qualitative Study. PLoS One 2016;11: e0164033. doi: 10.1371/journal.pone.0164033 27992427
11. Marangoni A, Foschi C, Nardini P, Compri M, Cevenini R. Evaluation of the Versant CT/GC DNA 1.0 assay (kPCR) for the detection of extra-genital Chlamydia trachomatis and Neisseria gonorrhoeae infections. PLoS One. 2015;10: e0120979. doi: 10.1371/journal.pone.0120979 25799263
12. Ceccarani C, Marangoni A, Severgnini M, Camboni T, Laghi L, Gaspari V, et al. Rectal Microbiota Associated With Chlamydia trachomatis and Neisseria gonorrhoeae Infections in Men Having Sex With Other Men. Front Cell Infect Microbiol 2019;9: 358. doi: 10.3389/fcimb.2019.00358 31681634
13. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinformatics. 2012;13: 31. doi: 10.1186/1471-2105-13-31 22333067
14. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7: 335–336. doi: 10.1038/nmeth.f.303 20383131
15. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73: 5261–5267 doi: 10.1128/AEM.00062-07 17586664
16. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, et al. Package “Vegan”. R Package Version 2.0–10. 2013; available online at: https://cran.r-project.org/src/contrib/Archive/vegan/vegan_2.0-10.tar.gz
17. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31: 814–821. doi: 10.1038/nbt.2676 23975157
18. Kaneisha M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acid Res. 2017;45: D353–D361. doi: 10.1093/nar/gkw1092 27899662
19. Kanehisa M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004;32: D277–D280. doi: 10.1093/nar/gkh063 14681412
20. Ceccarani C, Foschi C, Parolin C, D'Antuono A, Gaspari V, Consolandi C, et al. Diversity of vaginal microbiome and metabolome during genital infections. Sci Rep 2019;9: 14095. doi: 10.1038/s41598-019-50410-x 31575935
21. Laver JR, Hughes SE, Read RC. Neisserial Molecular Adaptations to the Nasopharyngeal Niche. Adv Microb Physiol. 2015;66: 323–355. doi: 10.1016/bs.ampbs.2015.05.001 26210107
22. Donati C, Zolfo M, Albanese D, Tin Truong D, Asnicar F, Iebba V, et al. Uncovering oral Neisseria tropism and persistence using metagenomic sequencing. Nat Microbiol. 2016;1: 16070. doi: 10.1038/nmicrobiol.2016.70 27572971
23. Weyand NJ. Neisseria models of infection and persistence in the upper respiratory tract. Pathog Dis. 2017;75(3).
24. Deasy AM, Guccione E, Dale AP, Andrews N, Evans CM, Bennett JS, et al. Nasal Inoculation of the Commensal Neisseria lactamica Inhibits Carriage of Neisseria meningitidis by Young Adults: A Controlled Human Infection Study.Clin Infect Dis. 2015;60: 1512–1520. doi: 10.1093/cid/civ098 25814628
25. Law DJ, Dajani AS. Interactions between Neisseria sicca and viridin B, a bacteriocin produced by Streptococcus mitis. Antimicrob Agents Chemother. 1978;13: 473–478. doi: 10.1128/aac.13.3.473 263887
26. Schielke S, Frosch M, Kurzai O. Virulence determinants involved in differential host niche adaptation of Neisseria meningitidis and Neisseria gonorrhoeae. Med Microbiol Immunol. 2010;199: 185–196. doi: 10.1007/s00430-010-0150-5 20379743
27. Mellies J, Rudel T, Meyer TF. Transcriptional regulation of pilC2 in Neisseria gonorrhoeae: response to oxygen availability and evidence for growth-phase regulation in Escherichia coli. Mol Gen Genet. 1997;255: 285–293. doi: 10.1007/s004380050499 9268019
28. Householder TC, Belli WA, Lissenden S, Cole JA, Clark VL. cis- and trans- acting elements involved in the regulation of aniA, the gene encoding the major anaerobically induced outer membrane protein in Nesseria gonorrhoeae. J Bacteriol. 1999;181: 5411–5551
29. Exley RM, Goodwin L, Mowe E, Shaw J, Smith H, Read RC, et al. Neisseria meningitidis lactate permease is required for nasopharyngeal colonization. Infect Immun. 2005;73: 5762–5766. doi: 10.1128/IAI.73.9.5762-5766.2005 16113293
30. Catenazzi MC, Jones H, Wallace I, Clifton J, Chong JP, Jackson MA, et al. A large genomic island allows Neisseria meningitidis to utilize propionic acid, with implications for colonization of the human nasopharynx. Mol Microbiol. 2014;93: 346–355. doi: 10.1111/mmi.12664 24910087
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