{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T08:20:04Z","timestamp":1790842804916,"version":"4.1.0"},"reference-count":80,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2022,2,19]],"date-time":"2022-02-19T00:00:00Z","timestamp":1645228800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>The female reproductive tract (FRT) microbiome plays a vital role in maintaining vaginal health. Viruses are key regulators of other microbial ecosystems, but little is known about how the FRT viruses (virome), particularly bacteriophages that comprise the phageome, impact FRT health and dysbiosis. We hypothesize that bacterial vaginosis (BV) is associated with altered FRT phageome diversity, transkingdom interplay, and bacteriophage discriminate taxa. Here, we conducted a retrospective, longitudinal analysis of vaginal swabs collected from 54 BV-positive and 46 BV-negative South African women. Bacteriome analysis revealed samples clustered into five distinct bacterial community groups (CGs), and further, bacterial alpha diversity was significantly associated with BV. Virome analysis on a subset of baseline samples showed FRT bacteriophages clustering into novel viral state types (VSTs), a viral community clustering system based on virome composition and abundance. Distinct BV bacteriophage signatures included increased alpha diversity along with discriminant Bacillus, Burkholderia, and Escherichia bacteriophages. Bacteriophage-bacteria transkingdom associations were also identified between Bacillus and Burkholderia viruses and BV-associated bacteria, providing key insights for future studies elucidating the transkingdom interactions driving BV-associated microbiome perturbations. In this cohort, bacteriophage-bacterial associations suggest complex interactions, which may play a role in the establishment and maintenance of BV.<\/jats:p>","DOI":"10.3390\/v14020430","type":"journal-article","created":{"date-parts":[[2022,2,21]],"date-time":"2022-02-21T08:34:47Z","timestamp":1645432487000},"page":"430","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Transkingdom Analysis of the Female Reproductive Tract Reveals Bacteriophages form Communities"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7710-3444","authenticated-orcid":false,"given":"Ferralita S.","family":"Madere","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Sohn","sequence":"additional","affiliation":[{"name":"Department of Biostatistics and Computational Biology, University of Rochester Medical Center, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angelina K.","family":"Winbush","sequence":"additional","affiliation":[{"name":"Division of Internal Medicine, University of Rochester School of Medicine & Dentistry, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bre\u00f3na","family":"Barr","sequence":"additional","affiliation":[{"name":"Department of Rural Family Medicine, West Virginia University, Morgantown, WV 25425, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alex","family":"Grier","sequence":"additional","affiliation":[{"name":"UR Genomics Research Center, University of Rochester Medical Center, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3468-3754","authenticated-orcid":false,"given":"Cal","family":"Palumbo","sequence":"additional","affiliation":[{"name":"UR Genomics Research Center, University of Rochester Medical Center, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James","family":"Java","sequence":"additional","affiliation":[{"name":"UR Genomics Research Center, University of Rochester Medical Center, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tracy","family":"Meiring","sequence":"additional","affiliation":[{"name":"Institute of Infectious Diseases & Molecular Medicine and Division of Medical Virology, Faculty of Health Sciences, University of Cape Town, Anzio Road, Observatory, Cape Town 7925, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5467-1200","authenticated-orcid":false,"given":"Anna-Lise","family":"Williamson","sequence":"additional","affiliation":[{"name":"Institute of Infectious Diseases & Molecular Medicine and Division of Medical Virology, Faculty of Health Sciences, University of Cape Town, Anzio Road, Observatory, Cape Town 7925, South Africa"},{"name":"South African Medical Research Council Gynaecological Cancer Research Centre, Faculty of Health Sciences, University of Cape Town, Cape Town 7505, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda-Gail","family":"Bekker","sequence":"additional","affiliation":[{"name":"Desmond Tutu HIV Centre, Institute of Infectious Diseases & Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Anzio Road, Observatory, Cape Town 7925, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8797-1621","authenticated-orcid":false,"given":"David H.","family":"Adler","sequence":"additional","affiliation":[{"name":"Department of Emergency Medicine, University of Rochester Medical Center, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3093-5563","authenticated-orcid":false,"given":"Cynthia L.","family":"Monaco","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, NY 14642, USA"},{"name":"Department of Internal Medicine, Division of Infectious Diseases, University of Rochester Medical Center, Rochester, NY 14642, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.coviro.2021.10.010","article-title":"The female reproductive tract virome: Understanding the dynamic role of viruses in gynecological health and disease","volume":"52","author":"Madere","year":"2021","journal-title":"Curr. Opin. Virol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"14095","DOI":"10.1038\/s41598-019-50410-x","article-title":"Diversity of vaginal microbiome and metabolome during genital infections","volume":"9","author":"Ceccarani","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1111\/1574-6976.12029","article-title":"Vaginal microbiota and its role in HIV transmission and infection","volume":"37","author":"Petrova","year":"2013","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.immuni.2016.12.013","article-title":"Lactobacillus-Deficient Cervicovaginal Bacterial Communities Are Associated with Increased HIV Acquisition in Young South African Women","volume":"46","author":"Gosmann","year":"2017","journal-title":"Immunity"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/j.ajog.2018.11.1089","article-title":"Ecological dynamics of the vaginal microbiome in relation to health and disease","volume":"220","author":"Greenbaum","year":"2019","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2519","DOI":"10.1007\/s10815-021-02247-5","article-title":"The impact of the female genital tract microbiome in women health and reproduction: A review","volume":"38","author":"Labarta","year":"2021","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_7","first-page":"1303265","article-title":"Changes in vaginal community state types reflect major shifts in the microbiome","volume":"28","author":"Brooks","year":"2017","journal-title":"Microb. Ecol. Health Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1113\/JP271694","article-title":"The vaginal microbiota, host defence and reproductive physiology","volume":"595","author":"Smith","year":"2017","journal-title":"J. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4680","DOI":"10.1073\/pnas.1002611107","article-title":"Vaginal microbiome of reproductive-age women","volume":"108","author":"Ravel","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_10","first-page":"443","article-title":"Vaginal microbiota and viral sexually transmitted diseases","volume":"25","author":"Nardis","year":"2013","journal-title":"Ann. Ig."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"131243","DOI":"10.1155\/2012\/131243","article-title":"The Microbiological Context of HIV Resistance: Vaginal Microbiota and Mucosal Inflammation at the Viral Point of Entry","volume":"2012","author":"Schellenberg","year":"2012","journal-title":"Int. J. Inflamm."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"4377","DOI":"10.1182\/blood-2009-09-245464","article-title":"Latent herpesvirus infection arms NK cells","volume":"115","author":"White","year":"2010","journal-title":"Blood"},{"key":"ref_13","first-page":"1968","article-title":"Bacterial vaginosis","volume":"13","author":"Joesoef","year":"2005","journal-title":"Clin. Evid."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Bilardi, J.E., Walker, S., Temple-Smith, M., McNair, R., Mooney-Somers, J., Bellhouse, C., Fairley, C.K., Chen, M.Y., and Bradshaw, C. (2013). The burden of bacterial vaginosis: Women\u2019s experience of the physical, emotional, sexual and social impact of living with recurrent bacterial vaginosis. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0074378"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1097\/OLQ.0b013e3182267ac4","article-title":"Effects of bacterial vaginosis-associated bacteria and sexual intercourse on vaginal colonization with the probiotic Lactobacillus crispatus CTV-05","volume":"38","author":"Ngugi","year":"2011","journal-title":"Sex. Transm. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Srinivasan, S., Liu, C., Mitchell, C.M., Fiedler, T.L., Thomas, K.K., Agnew, K.J., Marrazzo, J., and Fredricks, D.N. (2010). Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0010197"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1136\/sti.2009.040592","article-title":"Rapid fluctuation of the vaginal microbiota measured by Gram stain analysis","volume":"86","author":"Brotman","year":"2010","journal-title":"Sex. Transm. Infect."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.cell.2014.02.032","article-title":"The virome in mammalian physiology and disease","volume":"157","author":"Virgin","year":"2014","journal-title":"Cell"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1016\/j.immuni.2015.05.003","article-title":"The virome in host health and disease","volume":"42","author":"Cadwell","year":"2015","journal-title":"Immunity"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"189.e1","DOI":"10.1016\/j.ajog.2018.04.048","article-title":"The vaginal eukaryotic DNA virome and preterm birth","volume":"219","author":"Wylie","year":"2018","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Wylie, K.M., Mihindukulasuriya, K.A., Zhou, Y., Sodergren, E., Storch, G.A., and Weinstock, G.M. (2014). Metagenomic analysis of double-stranded DNA viruses in healthy adults. BMC Biol., 12.","DOI":"10.1186\/s12915-014-0071-7"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"559","DOI":"10.3389\/fmicb.2017.00559","article-title":"Intriguing Interaction of Bacteriophage-Host Association: An Understanding in the Era of Omics","volume":"8","author":"Parmar","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Lawrence, D., Baldridge, M.T., and Handley, S.A. (2019). Phages and Human Health: More Than Idle Hitchhikers. Viruses, 11.","DOI":"10.3390\/v11070587"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Fillol-Salom, A., Alsaadi, A., De Sousa, J.A.M., Zhong, L., Foster, K.R., Rocha, E.P.C., Penad\u00e9s, J.R., Ingmer, H., and Haaber, J. (2019). Bacteriophages benefit from generalized transduction. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1007888"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Jakobsen, R.R., Haahr, T., Humaidan, P., Jensen, J.S., Kot, W.P., Castro-Mejia, J.L., Deng, L., Leser, T.D., and Nielsen, D.S. (2020). Characterization of the Vaginal DNA Virome in Health and Dysbiosis. Viruses, 12.","DOI":"10.3390\/v12101143"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Happel, A.U., Balle, C., Maust, B.S., Konstantinus, I.N., Gill, K., Bekker, L.-G., Froissart, R., Passmore, J.-A., Karaoz, U., and Varsani, A. (2021). Presence and Persistence of Putative Lytic and Temperate Bacteriophages in Vaginal Metagenomes from South African Adolescents. Viruses, 13.","DOI":"10.3390\/v13122341"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"202","DOI":"10.5897\/JAHR2017.0445","article-title":"Human papillomavirus clustering patterns among HIV-infected and HIV-uninfected adolescent females in South Africa","volume":"9","author":"Dylla","year":"2017","journal-title":"J. AIDS HIV Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/2049-2618-2-6","article-title":"An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform","volume":"2","author":"Fadrosh","year":"2014","journal-title":"Microbiome"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME allows analysis of high-throughput community sequencing data","volume":"7","author":"Caporaso","year":"2010","journal-title":"Nat. Methods"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1038\/s41587-019-0209-9","article-title":"Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2","volume":"37","author":"Bolyen","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nmeth.3869","article-title":"DADA2: High-resolution sample inference from Illumina amplicon data","volume":"13","author":"Callahan","year":"2016","journal-title":"Nat. Methods"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5069","DOI":"10.1128\/AEM.03006-05","article-title":"Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB","volume":"72","author":"DeSantis","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT multiple sequence alignment software version 7: Improvements in performance and usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Price, M.N., Dehal, P.S., and Arkin, A.P. (2010). FastTree 2\u2014Approximately maximum-likelihood trees for large alignments. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009490"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1038\/ismej.2010.133","article-title":"UniFrac: An effective distance metric for microbial community comparison","volume":"5","author":"Lozupone","year":"2011","journal-title":"ISME J."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1186\/s40168-020-00934-6","article-title":"VALENCIA: A nearest centroid classification method for vaginal microbial communities based on composition","volume":"8","author":"France","year":"2020","journal-title":"Microbiome"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1812","DOI":"10.1128\/JCM.00851-09","article-title":"Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis","volume":"48","author":"Lillis","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.ijid.2015.02.009","article-title":"High risk human papillomavirus persistence among HIV-infected young women in South Africa","volume":"33","author":"Adler","year":"2015","journal-title":"Int. J. Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e2159","DOI":"10.21769\/BioProtoc.2159","article-title":"Next-generation Sequencing of the DNA Virome from Fecal Samples","volume":"7","author":"Monaco","year":"2017","journal-title":"Bio. Protoc."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.virol.2017.01.005","article-title":"VirusSeeker, a computational pipeline for virus discovery and virome composition analysis","volume":"503","author":"Zhao","year":"2017","journal-title":"Virology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1093\/bioinformatics\/btx754","article-title":"bioBakery: A meta\u2019omic analysis environment","volume":"34","author":"McIver","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1674","DOI":"10.1093\/bioinformatics\/btv033","article-title":"MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph","volume":"31","author":"Li","year":"2015","journal-title":"Bioinformatics"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010). Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform., 11.","DOI":"10.1186\/1471-2105-11-119"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"W29","DOI":"10.1093\/nar\/gkr367","article-title":"HMMER web server: Interactive sequence similarity searching","volume":"39","author":"Finn","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"D491","DOI":"10.1093\/nar\/gkw975","article-title":"Prokaryotic Virus Orthologous Groups (pVOGs): A resource for comparative genomics and protein family annotation","volume":"45","author":"Grazziotin","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Pinheiro, J.C., and Bates, D.M. (2000). Mixed-Effects Models in S and S-PLUS, Springer.","DOI":"10.1007\/978-1-4419-0318-1"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/j.chom.2016.02.011","article-title":"Altered Virome and Bacterial Microbiome in Human Immunodeficiency Virus-Associated Acquired Immunodeficiency Syndrome","volume":"19","author":"Monaco","year":"2016","journal-title":"Cell Host Microbe"},{"key":"ref_48","first-page":"237ra65","article-title":"The placenta harbors a unique microbiome","volume":"6","author":"Aagaard","year":"2014","journal-title":"Sci. Transl. Med."},{"key":"ref_49","first-page":"32","article-title":"A new method for non-parametric multivariate analysis of variance","volume":"26","author":"Anderson","year":"2001","journal-title":"Austral. Ecol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Kaufmann, L., and Rousseeuw, P.J. (1990). Finding Groups in Data: An Introduction to Cluster Analysis, John Wiley & Sons.","DOI":"10.1002\/9780470316801"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1093\/biomet\/30.1-2.81","article-title":"A New Measure of Rank Correlation","volume":"30","author":"Kendall","year":"1938","journal-title":"Biometrika"},{"key":"ref_52","unstructured":"(2020). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: A practical and powerful approach to multiple testing","volume":"57","author":"Hochberg","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Torcia, M.G. (2019). Interplay among Vaginal Microbiome, Immune Response and Sexually Transmitted Viral Infections. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20020266"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1016\/j.immuni.2015.04.019","article-title":"Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract","volume":"42","author":"Anahtar","year":"2015","journal-title":"Immunity"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e00342-18","DOI":"10.1128\/JCM.00342-18","article-title":"Molecular Diagnosis of Bacterial Vaginosis: An Update","volume":"56","author":"Coleman","year":"2018","journal-title":"J. Clin. Microbiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e00984-13","DOI":"10.1128\/genomeA.00984-13","article-title":"Complete Genome of Bacillus subtilis Myophage CampHawk","volume":"1","author":"Ritz","year":"2013","journal-title":"Genome Announc."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Grose, J.H., Jensen, G.L., Burnett, S.H., and Breakwell, D.P. (2014). Correction: Genomic comparison of 93 Bacillus phages reveals 12 clusters, 14 singletons and remarkable diversity. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-1184"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/j.meegid.2016.08.001","article-title":"Identification of vaginal bacteria diversity and its association with clinically diagnosed bacterial vaginosis by denaturing gradient gel electrophoresis and correspondence analysis","volume":"44","author":"Xia","year":"2016","journal-title":"Infect. Genet. Evol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"81","DOI":"10.3389\/fphys.2015.00081","article-title":"Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health","volume":"6","author":"Petrova","year":"2015","journal-title":"Front. Physiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"27423","DOI":"10.3402\/jom.v7.27423","article-title":"Bacteriophage and their potential roles in the human oral cavity","volume":"7","author":"Edlund","year":"2015","journal-title":"J. Oral Microbiol."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Willms, I.M., Hoppert, M., and Hertel, R. (2017). Characterization of Bacillus Subtilis Viruses vB_BsuM-Goe2 and vB_BsuM-Goe3. Viruses, 9.","DOI":"10.3390\/v9060146"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"e00860-13","DOI":"10.1128\/genomeA.00860-13","article-title":"Complete Genome of Bacillus megaterium Podophage Pony","volume":"1","author":"Khatemi","year":"2013","journal-title":"Genome Announc."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1334","DOI":"10.1111\/jam.13690","article-title":"Bacillus probiotics: An alternative to antibiotics for livestock production","volume":"124","author":"Mingmongkolchai","year":"2018","journal-title":"J. Appl. Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1016\/j.meegid.2007.01.005","article-title":"Experimental coevolution with bacteria and phage. The Pseudomonas fluorescens\u2014Phi2 model system","volume":"7","author":"Brockhurst","year":"2007","journal-title":"Infect. Genet. Evol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/S0966-842X(98)01320-1","article-title":"Bacteriophage biology and bacterial virulence","volume":"6","author":"Waldor","year":"1998","journal-title":"Trends Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1038\/s41385-019-0250-5","article-title":"New insights into intestinal phages","volume":"13","author":"Sausset","year":"2020","journal-title":"Mucosal Immunol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1124","DOI":"10.1016\/j.ajog.2004.05.033","article-title":"Antimicrobial resistance associated with the treatment of bacterial vaginosis","volume":"191","author":"Beigi","year":"2004","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_69","first-page":"155","article-title":"Antibiotic resistance of Gardnerella vaginalis in recurrent bacterial vaginosis","volume":"26","author":"Nagaraja","year":"2008","journal-title":"Indian J. Med. Microbiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1086\/509584","article-title":"Bacterial vaginosis: Resistance, recurrence, and\/or reinfection?","volume":"44","author":"Eschenbach","year":"2007","journal-title":"Clin. Infect. Dis."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"97.e1","DOI":"10.1016\/j.ajog.2007.06.039","article-title":"An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole","volume":"198","author":"Swidsinski","year":"2008","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1111\/j.1365-2672.2011.04977.x","article-title":"The aetiology of bacterial vaginosis","volume":"110","author":"Turovskiy","year":"2011","journal-title":"J. Appl. Microbiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1484","DOI":"10.1128\/jb.178.5.1484-1486.1996","article-title":"Proteins responsible for lysogenic conversion caused by coliphages N15 and phi80 are highly homologous","volume":"178","author":"Vostrov","year":"1996","journal-title":"J. Bacteriol."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Pleckaityte, M., Zilnyte, M., and Zvirbliene, A. (2012). Insights into the CRISPR\/Cas system of Gardnerella vaginalis. BMC Microbiol., 12.","DOI":"10.1186\/1471-2180-12-301"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Rho, M., Wu, Y.W., Tang, H., Doak, T.G., and Ye, Y. (2012). Diverse CRISPRs evolving in human microbiomes. PLoS Genet., 8.","DOI":"10.1371\/journal.pgen.1002441"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/2049-2618-1-12","article-title":"Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis","volume":"1","author":"Macklaim","year":"2013","journal-title":"Microbiome"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1099\/jmm.0.024463-0","article-title":"Identification of predominant culturable vaginal Lactobacillus species and associated bacteriophages from women with and without vaginal discharge syndrome in South Africa","volume":"60","author":"Damelin","year":"2011","journal-title":"J. Med. Microbiol."},{"key":"ref_78","first-page":"131","article-title":"Bacteriophage induction versus vaginal homeostasis: Role of H2O2 in the selection of Lactobacillus defective prophages","volume":"12","author":"Escobedo","year":"2009","journal-title":"Int. Microbiol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1128\/CDLI.8.1.31-39.2001","article-title":"Comparative study of vaginal Lactobacillus phages isolated from women in the United States and Turkey: Prevalence, morphology, host range, and DNA homology","volume":"8","author":"Kilic","year":"2001","journal-title":"Clin. Diagn. Lab. Immunol."},{"key":"ref_80","first-page":"36","article-title":"Phage infection in vaginal Lactobacilli: An in vitro study","volume":"5","author":"Pavlova","year":"1997","journal-title":"Infect. Dis. Obstet. Gynecol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/2\/430\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:23:07Z","timestamp":1760134987000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/2\/430"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,19]]},"references-count":80,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["v14020430"],"URL":"https:\/\/doi.org\/10.3390\/v14020430","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.10.12.464088","asserted-by":"object"}]},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,19]]}}}