Journal of microbiology, epidemiology and immunobiologyJournal of microbiology, epidemiology and immunobiology0372-93112686-7613Central Research Institute for Epidemiology98510.36233/0372-9311-53Unknown<i>Moraxella osloensis</i> as a part of genital tract microbiota in infertility: incidental findings or pathology markers?GodovalovA. P.<p>Anatoliy P. Godovalov — PhD (Med.), leading researcher, Central scientific research laboratory, Assoc. Prof., Microbiology and virology department</p><p>Perm</p>agodovalov@gmail.comhttps://orcid.org/0000-0002-5112-2003KarpuninaN. S.<p>Natalia S. Karpunina — D. Sci. (Med.), Prof., Hospital therapy and cardiology department</p><p>Perm</p>fake@neicon.ruhttps://orcid.org/0000-0003-3127-1797KarpuninaT. I.<p>Tamara I. Karpunina — D. Sci. (Biol.), Prof., Microbiology and virology department</p><p>Perm</p>fake@neicon.ruhttps://orcid.org/0000-0003-2511-4656E.A. Vagner Perm State Medical University0403202198128350303202103032021Copyright © 2021, Godovalov A.P., Karpunina N.S., Karpunina T.I.2021<p><strong>Aim</strong>. To assess the potential role of <em>M. osloensis</em> in genital microbiota of infertile males and females..<br /><strong>Materials and methods</strong>. Samples from mens urethra and womens posterior vaginal fornix in barren couples of the reproductive age were examined. Cultivation was carried out using elective culture media with subsequent identification of strains by biochemical properties. A metagenomic study of <em>16S</em> ribosomal RNA samples was performed on the Illumina MiSeq platform using the MiSeq Reagent Kits v3 kit (600-Cycle Kit).<br /><strong>Results</strong>. Metagenomic study of samples from genital tracts of barren married couples, as well as from patients with suspected acute genital gonococcal infection demonstrated that all samples (100%) contained fragments of the <em>Moraxella spp.</em> genome, mostly in a huge amount, among which <em>M. osloensis</em> occupied leading positions. In women, the proportion of <em>M. osloensis</em> was twice as large as in men (25.3 9.0 and 11.7 9.3%, respectively). A high frequency of association of <em>M. osloensis</em> with other opportunistic pathogens, <em>G. vaginalis</em> and <em>E. faecalis</em> in particular, was established. It appears that <em>M. osloensis</em> can contribute to development of asymptomatic inflammatory process. Moreover, the constant presence of moraxellas in the microbiota during gonococcal infection may indicate their certain pathogenetic activity, and the synergistic nature of the relationship between <em>M. osloensis</em> and <em>N. gonorrhoeae</em>.<br /><strong>Conclusion</strong>. We assume that it is <em>M. osloensis</em> that forms the consortia determining pathosymbiocenosis in the reproductive organs. In this context, we propose to consider a decrease in fertility with a steadily established symbiocenosis, including moraxella, as an indicative condition for this pathology, and <em>M. osloensis</em> as its marker.</p>microbiome investigation16S RNA sequencingM. osloensispathosymbiocenosisinfertilitymarkerисследование микробиома16S РНК секвенированиеM. osloensisпатосимбиоценозбесплодиемаркер[Kamińska D., Gajecka М. Is the role of human female reproductive tract microbiota underestimated? Benef. Microbes. 2017; 8(3): 327–43. https://doi.org/10.3920/BM2015.0174][Buchta V. Vaginal microbiome. Ceska Gynekol. Winter. 2018; 83(5): 371–9.][Gardner H.L., Dukes C.D. Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified non-specific vaginitis. Am. J. Obstet. Gynecol. 1955; 69(5): 962–76.][Piot P., Van Dyck E., Totten P.A., Holmes K.K. Identification of Gardnerella (Haemophilus) vaginalis. J. Clin. Microbiol. 1982; 15(1): 19–24. https://doi.org/10.1128/jcm.15.1.19-24.1982][Machado A., Cerca N. Influence of biofilm formation by Gardnerella vaginalis and other anaerobes on bacterial vaginosis. J. Infect. Dis. 2015; 212(12): 1856–61. https://doi.org/10.1093/infdis/jiv338][Damke E., Kurscheidt F.A., Irie M.M.T., Gimenes F., Consolaro M.E.L. Male partners of infertile couples with seminal positivity for markers of bacterial vaginosis have impaired fertility. Am. J. Mens. Health. 2018; 12(6): 2104–15. https://doi.org/10.1177/1557988318794][Ravel J., Gajer P., Abdo Z., Schneider G.M., Koenig S.S., McCulle S.L., et al. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. USA. 2011; 108(Suppl. 1): 4680–7. https://doi.org/10.1073/pnas.1002611107][Martin D.H., Marrazzo J.M. The vaginal microbiome: current understanding and future directions. J. Infect. Dis. 2016; 214(Suppl. 1): S36–41. https://doi.org/10.1093/infdis/jiw184][Martin D.H., Zozaya M., Lillis R., Miller J., Ferris M.J. The microbiota of the human genitourinary tract: trying to see the forest through the trees. Trans. Am. Clin. Climatol. Assoc. 2012; 123: 242–56.][Hong X., Fang S., Huang K., Yin J., Chen J., Xuan Y., et al. Characteristics of the vaginal microbiome in cross-border female sex workers in China: a case-control study. PeerJ. 2019; 7: e8131. https://doi.org/10.7717/peerj.8131][Li F., Chen C., Wei W., Wang Z., Dai J., Hao L., et al. The metagenome of the female upper reproductive tract. Gigascience. 2018; 7(10): giy107. http://doi.org/10.1093/gigascience/giy107][Morax V. Note sur un diplobacille pathogéne pour la conjunctivite humaine. Ann. Inst. Pasteur. 1896; 10: 337–45.][LaCroce S.J., Wilson M.N., Romanowski J.E., Newman J.D., Jhanji V., Shanks R.M.Q., et al. Moraxella nonliquefaciens and M. osloensis are important Moraxella species that cause ocular infections. Microorganisms. 2019; 7(6): 163. https://doi.org/10.3390/microorganisms7060163][Henriksen S.D. Moraxella, Acinetobacter, and the Mimeae. Bacteriol. Rev. 1973; 37(4): 522–61.][Riley P.S., Hollis D.G., Weaver R.E. Characterization and differentiation of 59 strains of Moraxella urethralis from clinical specimens. Appl. Microbiol. 1974; 28(3): 355–8.][Abdolrasouli A., Amin A., Baharsefat M., Roushan A., Hemmati Y. Moraxella catarrhalis associated with acute urethritis imitating gonorrhoea acquired by oral-genital contact. Int. J. STD AIDS. 2007; 18(8): 579–80. http://doi.org/10.1258/095646207781439775][Gómez-Camarasa C., Fernández-Parra J., Navarro-Marí J.M., Gutiérrez-Fernández J. Moraxella osloensis emerging infection. Visiting to genital infection. Rev. Esp. Quimioter. 2018; 31(2): 178–81. (in Spanish)][Coker D.M., Griffiths L.R. Moraxella urethritis mimicking gonorrhoea. Genitourin. Med. 1991; 67(2): 173–4. http://doi.org/10.1136/sti.67.2.173-a][Богун А.Г., Кисличкина А.А., Галкина Е.В., Майская Н.В., Соломенцев В.И., Мухина Т.Н. и др. Использование современных методов идентификации бактерий в деятельности государственной коллекции патогенных микроорганизмов и клеточных культур (ГКПМ-Оболенск). Инфекция и иммунитет. 2016; 6(3): 8.][Shaffer M., Armstrong A.J.S., Phelan V.V., Reisdorph N., Lozupone C.A. Microbiome and metabolome data integration provides insight into health and disease. Transl. Res. 2017; 189: 51–64. https://doi.org/10.1016/j.trsl.2017.07.001][Кубанов А.А., Барышков К.В., Честков А.В., Шаскольский Б.Л., Грудянов Д.А., Дерябин Д.Г. Генотипическое разнообразие популяции Neisseria gonorrhoeae в Архангельске (Россия): механизмы формирования и связь с устойчивостью к антимикробным препаратам. Молекулярная генетика, микробиология и вирусология. 2018; 36(3): 43–8. http://doi.org/10.17116/molgen20183603143][Di Capua C., Bortolotti A., Farías M.E., Cortez N. UV-resistant Acinetobacter sp. isolates from Andean wetlands display high catalase activity. FEMS Microbiol. Lett. 2011; 317(2): 181–9. https://doi.org/10.1111/j.1574-6968.2011.02231.x][Kubota H., Mitan A., Niwano Y., Takeuch K., Tanaka A., Yamaguchi N., et al. Moraxella species are primarily responsible for generating malodor in laundry. Appl. Environ. Microbiol. 2012; 78(9): 3317–24. https://doi.org/10.1128/aem.07816-11][Beney L., Gervais P. Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl. Microbiol. Biotechnol. 2001; 57(1-2): 34–42. https://doi.org/10.1007/s002530100754][Sugimoto C., Miyagawa E., Nakazawa M., Mitani K., Ishizawa Y. Cellular fatty acid composition comparisons of Haemophilus equigenitalis and Moraxella species. Int. J. Syst. Bacteriol. 1983; 33(2): 181–7. https://doi.org/10.1099/00207713-33-2-181][Tan L., Grewal P.S. Endotoxin activity of Moraxella osloensis against the grey garden slug, Deroceras reticulatum. Appl. Environ. Microbiol. 2002; 68(8): 3943–7. http://doi.org/10.1128/aem.68.8.3943-3947.2002][Баранова Е.Д., Дружинин В.Г. Состав бактериальной микрофлоры человека: генотоксические и канцерогенные эффекты, ассоциированные с его изменениями в различных органах. Молекулярная генетика, микробиология и вирусология. 2019; 37(2): 58–63. https://doi.org/10.17116/molgen20193702158][Cerca N., Vaneechoutte M., Guschin A., Swidsinski A. Polymicrobial infections and biofilms in women's health: Gahro Expert Group Meeting Report. Res. Microbiol. 2017; 168(9-10): 902–4. http://doi.org/10.1016/j.resmic.2017.07.002][Khan S., Voordouw M.J., Hill J.E. Competition among Gardnerella subgroups from the human vaginal microbiome. Front. Cell. Infect. Microbiol. 2019; 9: 374. http://doi.org/10.3389/fcimb.2019.00374][Hill J.E., Albert A.Y.K., VOGUE Research Group. Resolution and сooccurrence patterns of Gardnerella leopoldii, G. swidsinskii, G. piotii, and G. vaginalis within the vaginal microbiome. Infect. Immun. 2019; 87(12): e00532-19. http://doi.org/10.1128/IAI.00532-19][Castro J., Jefferson K.K., Cerca N. Genetic heterogeneity and taxonomic diversity among Gardnerella species. Trends Microbiol. 2020; 28(3): 202–11. http://doi.org/10.1016/j.tim.2019.10.002][Nisha K., Antony B., Udayalaxmi J. Comparative analysis of virulence factors & biotypes of Gardnerella vaginalis isolated from the genital tract of women with & without bacterial vaginosis. Indian. J. Med. Res. 2019; 149(1): 57–61. http://doi.org/10.4103/ijmr.IJMR_1674_16][Савичева А.М., Крысанова А.А., Лищук О.В. Единственная в своём роде? StatusPraesens. Гинекология, акушерство, бесплодный брак. 2019; (5): 32–40.][Belkaid Y., Hand T.W. Role of the microbiota in immunity and inflammation. Cell. 2014; 157(1): 121–41. https://doi.org/10.1016/j.cell.2014.03.011]