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Volume 7, Issue 3

Genomic relatedness and clinical significance of strains isolated from the urogenital tract of sexual partners Open Access

Abstract

Research into the lower urinary tract (LUT) microbiota has primarily focused on its relationship to LUT symptoms (LUTS), taking snapshots of these communities in individuals with and without LUTS. While certain bacterial taxa have been associated with LUTS, or the lack thereof, the temporal dynamics of this community were largely unknown. Recently, we conducted a longitudinal study and found that vaginal intercourse resulted in a shift in species richness and diversity within the LUT microbiota. This is particularly relevant as frequent vaginal intercourse is a major risk factor for urinary tract infection (UTI) in premenopausal women (Aydin 2015;26:795–804). To further investigate the relationship between vaginal intercourse and LUT microbiota, here we present the results of a 3 week study in which daily urogenital specimens were collected from a female participant and her male sexual partner. Consistent with our previous findings, the LUT microbiota changed after vaginal intercourse, most notably a high abundance of was observed post-coitus. We isolated and sequenced from both sexual partners finding that: (i) the isolates from the female partner’s urogenital tract were genomically similar throughout the duration of the study, and (ii) they were related to one isolate from the male partner’s oral cavity collected at the end of the study, suggesting transmission between the two individuals. We hypothesize that blooms in after vaginal intercourse may play a role in coitus-related UTI. We found that a isolate, in contrast to a isolate displaced after vaginal intercourse, cannot inhibit the growth of uropathogenic . Thus, this bloom in may provide a window of opportunity for a uropathogen to colonize the LUT.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): lower urinary tract , metaculturomics , microbiome , sex , Streptococcus mitis and urinary microbiota
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2021-02-25
2024-04-19
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References

  1. Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ et al. Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol 2014; 52:871–876 [View Article][PubMed]
     [Google Scholar]
  2. Fouts DE, Pieper R, Szpakowski S, Pohl H, Knoblach S et al. Integrated next-generation sequencing of 16S rDNA and metaproteomics differentiate the healthy urine microbiome from asymptomatic bacteriuria in neuropathic bladder associated with spinal cord injury. J Transl Med 2012; 10:174 [View Article][PubMed]
     [Google Scholar]
  3. Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K et al. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol 2012; 50:1376–1383 [View Article][PubMed]
     [Google Scholar]
  4. Karstens L, Asquith M, Davin S, Stauffer P, Fair D et al. Does the urinary microbiome play a role in urgency urinary incontinence and its severity?. Front Cell Infect Microbiol 2016; 6:78 [View Article][PubMed]
     [Google Scholar]
  5. Pearce MM, Hilt EE, Rosenfeld AB, Zilliox MJ, Thomas-White K et al. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. mBio 2014; 5:e01283-14 [View Article][PubMed]
     [Google Scholar]
  6. Price TK, Wolff B, Halverson T, Limeira R, Brubaker L et al. Temporal dynamics of the adult female lower urinary tract microbiota. mBio 2020; 11:e00475-20 [View Article][PubMed]
     [Google Scholar]
  7. Siddiqui H, Lagesen K, Nederbragt AJ, Jeansson SL, Jakobsen KS. Alterations of microbiota in urine from women with interstitial cystitis. BMC Microbiol 2012; 12:205 [View Article][PubMed]
     [Google Scholar]
  8. Thomas-White KJ, Hilt EE, Fok C, Pearce MM, Mueller ER et al. Incontinence medication response relates to the female urinary microbiota. Int Urogynecol J 2016; 27:723–733 [View Article][PubMed]
     [Google Scholar]
  9. Abernethy MG, Rosenfeld A, White JR, Mueller MG, Lewicky-Gaupp C et al. Urinary microbiome and cytokine levels in women with interstitial cystitis. Obstet Gynecol 2017; 129:500–506 [View Article][PubMed]
     [Google Scholar]
  10. Thomas-White KJ, Kliethermes S, Rickey L, Lukacz ES, Richter HE et al. Evaluation of the urinary microbiota of women with uncomplicated stress urinary incontinence. Am J Obstet Gynecol 2017; 216:55.e1–55.e16 [View Article]
     [Google Scholar]
  11. Komesu YM, Richter HE, Carper B, Dinwiddie DL, Lukacz ES. The urinary microbiome in women with mixed urinary incontinence compared to similarly aged controls. Int Urogynecol J 2018; 29:1785–1795 [View Article][PubMed]
     [Google Scholar]
  12. Chen Z, Phan M, Bates LJ, Peters KM, Mukerjee C et al. The urinary microbiome in patients with refractory urge incontinence and recurrent urinary tract infection. Int Urogynecol J 2018; 29:1775–1782 [View Article][PubMed]
     [Google Scholar]
  13. Nickel JC, Stephens A, Landis JR, Mullins C, van Bokhoven A et al. Assessment of the lower urinary tract microbiota during symptom flare in women with urologic chronic pelvic pain syndrome: a MAPP network study. J Urol 2016; 195:356–362 [View Article][PubMed]
     [Google Scholar]
  14. Willner D, Low S, Steen JA, George N, Nimmo GR et al. Single clinical isolates from acute uncomplicated urinary tract infections are representative of dominant in situ populations. mBio 2014; 5:e01064-13 [View Article][PubMed]
     [Google Scholar]
  15. Dune TJ, Price TK, Hilt EE, Thomas-White KJ, Kliethermes S et al. Urinary symptoms and their associations with urinary tract infections in urogynecologic patients. Obstet Gynecol 2017; 130:718–725 [View Article][PubMed]
     [Google Scholar]
  16. Price TK, Hilt EE, Dune TJ, Mueller ER, Wolfe AJ et al. Urine trouble: should we think differently about UTI?. Int Urogynecol J 2018; 29:205–210 [View Article][PubMed]
     [Google Scholar]
  17. Curtiss N, Balachandran A, Krska L, Peppiatt-Wildman C, Wildman S et al. A case controlled study examining the bladder microbiome in women with overactive bladder (OAB) and healthy controls. Eur J Obstet Gynecol Reprod Biol 2017; 214:31–35 [View Article][PubMed]
     [Google Scholar]
  18. Groah SL, Pérez-Losada M, Caldovic L, Ljungberg IH, Sprague BM et al. Redefining healthy urine: a cross-sectional exploratory metagenomic study of people with and without bladder dysfunction. J Urol 2016; 196:579–587 [View Article][PubMed]
     [Google Scholar]
  19. Bresler L, Price TK, Hilt EE, Joyce C, Fitzgerald CM et al. Female lower urinary tract microbiota do not associate with IC/PBS symptoms: a case-controlled study. Int Urogynecol J 2019; 30:1835–1842 [View Article][PubMed]
     [Google Scholar]
  20. Jacobs KM, Price TK, Thomas-White K, Halverson T, Davies A. Cultivable bacteria in urine of women with interstitial cystitis: (not) what we expected. Female Pelvic Med Reconstr Surg [View Article]
     [Google Scholar]
  21. Moore EE, Hawes SE, Scholes D, Boyko EJ, Hughes JP et al. Sexual intercourse and risk of symptomatic urinary tract infection in post-menopausal women. J Gen Intern Med 2008; 23:595–599 [View Article][PubMed]
     [Google Scholar]
  22. Nicolle LE, Harding GK, Preiksaitis J, Ronald AR. The association of urinary tract infection with sexual intercourse. J Infect Dis 1982; 146:579–583 [View Article][PubMed]
     [Google Scholar]
  23. Buckley RM, McGuckin M, MacGregor RR. Urine bacterial counts after sexual intercourse. N Engl J Med 1978; 298:321–324 [View Article][PubMed]
     [Google Scholar]
  24. Foxman B, Somsel P, Tallman P, Gillespie B, Raz R et al. Urinary tract infection among women aged 40 to 65: behavioral and sexual risk factors. J Clin Epidemiol 2001; 54:710–718 [View Article][PubMed]
     [Google Scholar]
  25. Wolff BJ, Price TK, Joyce CJ, Wolfe AJ, Mueller ER. Oral probiotics and the female urinary microbiome: a double-blinded randomized placebo-controlled trial. Int Urol Nephrol 2019; 51:2149–2159 [View Article][PubMed]
     [Google Scholar]
  26. Mores CR, Price TK, Brassil B, Putonti C, Wolfe AJ. Complete genome sequences of Streptococcus mitis strains isolated from the oral cavity and urogenital tract of a woman and her male sexual partner. Microbiol Resour Announc 2020; 9:e01379-19 [View Article][PubMed]
     [Google Scholar]
  27. Price TK, Dune T, Hilt EE, Thomas-White KJ, Kliethermes S et al. The clinical urine culture: enhanced techniques improve detection of clinically relevant microorganisms. J Clin Microbiol 2016; 54:1216–1222 [View Article][PubMed]
     [Google Scholar]
  28. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
     [Google Scholar]
  29. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
     [Google Scholar]
  30. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114–5119 [View Article][PubMed]
     [Google Scholar]
  31. Richter M, Rossello-Mora R, Oliver Glockner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article][PubMed]
     [Google Scholar]
  32. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article][PubMed]
     [Google Scholar]
  33. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:132 [View Article][PubMed]
     [Google Scholar]
  34. Langermann S, Palaszynski S, Barnhart M, Auguste G, Pinkner JS et al. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 1997; 276:607–611 [View Article][PubMed]
     [Google Scholar]
  35. Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V et al. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci USA 2006; 103:5977–5982 [View Article][PubMed]
     [Google Scholar]
  36. Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC et al. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli . Science 1998; 282:1494–1497 [View Article][PubMed]
     [Google Scholar]
  37. Le PT, Pearce MM, Zhang S, Campbell EM, Fok CS et al. IL22 regulates human urothelial cell sensory and innate functions through modulation of the acetylcholine response, immunoregulatory cytokines and antimicrobial peptides: assessment of an in vitro model. PLoS One 2014; 9:e111375 [View Article][PubMed]
     [Google Scholar]
  38. Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW et al. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome 2014; 2:4 [View Article][PubMed]
     [Google Scholar]
  39. Martin R, Suarez JE. Biosynthesis and degradation of H2O2 by vaginal lactobacilli. Appl Environ Microbiol 2010; 76:400–405 [View Article][PubMed]
     [Google Scholar]
  40. Hertzberger R, Arents J, Dekker HL, Pridmore RD, Gysler C et al. H2O2 production in species of the Lactobacillus acidophilus group: a central role for a novel NADH-dependent flavin reductase. Appl Environ Microbiol 2014; 80:2229–2239 [View Article][PubMed]
     [Google Scholar]
  41. Sacks D, Baxter B, Campbell BCV, Carpenter JS, Cognard C. Multisociety consensus quality improvement revised consensus statement for endovascular therapy of acute ischemic stroke. Int J Stroke 2018; 13:612–632 [View Article][PubMed]
     [Google Scholar]
  42. Lewis FM, Bernstein KT, Aral SO. Vaginal microbiome and its relationship to behavior, sexual health, and sexually transmitted diseases. Obstet Gynecol 2017; 129:643–654 [View Article][PubMed]
     [Google Scholar]
  43. Cao X-W, Lin K, Li C-Y, Yuan C-W. [A review of WHO Laboratory Manual for the Examination and Processing of Human Semen (5th edition)]. Zhonghua Nan Ke Xue 2011; 17:1059–1063[PubMed]
     [Google Scholar]
  44. Price TK. Assessing the temporal dynamics of the lower urinary tract microbiota and the effects of lifestyle. PhD Thesis Loyola University; Chicago, USA: 2019
     [Google Scholar]
  45. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005; 102:2567–2572 [View Article][PubMed]
     [Google Scholar]
  46. Kilian M, Poulsen K, Blomqvist T, Håvarstein LS, Bek-Thomsen M et al. Evolution of Streptococcus pneumoniae and its close commensal relatives. PLoS One 2008; 3:e2683 [View Article][PubMed]
     [Google Scholar]
  47. Jensen A, Scholz CFP, Kilian M. Re-evaluation of the taxonomy of the Mitis group of the genus Streptococcus based on whole genome phylogenetic analyses, and proposed reclassification of Streptococcus dentisani as Streptococcus oralis subsp. dentisani comb. nov., Streptococcus tigurinus as Streptococcus oralis subsp. tigurinus comb. nov., and Streptococcus oligofermentans as a later synonym of Streptococcus cristatus . Int J Syst Evol Microbiol 2016; 66:4803–4820 [View Article][PubMed]
     [Google Scholar]
  48. Velsko IM, Perez MS, Richards VP. Resolving phylogenetic relationships for Streptococcus mitis and Streptococcus oralis through core- and pan-genome analyses. Genome Biol Evol 2019; 11:1077–1087 [View Article][PubMed]
     [Google Scholar]
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Genomic relatedness and clinical significance of Streptococcus mitis strains isolated from the urogenital tract of sexual partners
M Gen 7, 000535 (2021); https://doi.org/10.1099/mgen.0.000535
/content/journal/mgen/10.1099/mgen.0.000535
/content/journal/mgen/10.1099/mgen.0.000535
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