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Genome Investigation of Urinary Gardnerella Strains and Their Relationship to Isolates of the Vaginal Microbiota.

ABSTRACT: Gardnerella is a frequent member of the urogenital microbiota. Given the association between Gardnerella vaginalis and bacterial vaginosis (BV), significant efforts have been focused on characterizing this species in the vaginal microbiota. However, Gardnerella also is a frequent member of the urinary microbiota. In an effort to characterize the bacterial species of the urinary microbiota, we present here 10 genomes of urinary Gardnerella isolates from women with and without lower urinary tract symptoms. These genomes complement those of 22 urinary Gardnerella strains previously isolated and sequenced by our team. We included these genomes in a comparative genome analysis of all publicly available Gardnerella genomes, which include 33 urinary isolates, 78 vaginal isolates, and 2 other isolates. While once this genus was thought to consist of a single species, recent comparative genome analyses have revealed 3 new species and an additional 9 groups within Gardnerella Based upon our analysis, we suggest a new group for the species. We also find that distinction between these Gardnerella species/groups is possible only when considering the core or whole-genome sequence, as neither the sialidase nor vaginolysin genes are sufficient for distinguishing between species/groups despite their clinical importance. In contrast to the vaginal microbiota, we found that only five Gardnerella species/groups have been detected within the lower urinary tract. Although we found no association between a particular Gardnerella species/group(s) and urinary symptoms, further sequencing of urinary Gardnerella isolates is needed for both comprehensive taxonomic characterization and etiological classification of Gardnerella in the urinary tract.IMPORTANCE Prior research into the bacterium Gardnerella vaginalis has largely focused on its association with bacterial vaginosis (BV). However, G. vaginalis is also frequently found within the urinary microbiota of women with and without lower urinary tract symptoms as well as individuals with chronic kidney disease, interstitial cystitis, and BV. This prompted our investigation into Gardnerella from the urinary microbiota and all publicly available Gardnerella genomes from the urogenital tract. Our work suggests that while some Gardnerella species can survive in both the urinary tract and vagina, others likely cannot. This study provides the foundation for future studies of Gardnerella within the urinary tract and its possible contribution to lower urinary tract symptoms.

SUBMITTER: Putonti C

PROVIDER: S-EPMC8125048 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAlthough the vaginal and urinary microbiomes have been increasingly well-characterized in health and disease, few have described the relationship between these neighboring environments. Elucidating this relationship has implications for understanding how manipulation of the vaginal microbiome may affect the urinary microbiome and treatment of common urinary conditions.ObjectiveTo describe the relationship between urinary and vaginal microbiomes using 16S rRNA gene sequencing. We hypothesized that the composition of the urinary and vaginal microbiomes would be significantly associated, with similarities in predominant taxa.Study designThis multicenter study collected vaginal swabs and catheterized urine samples from 186 women with mixed urinary incontinence enrolled in a parent study and 84 similarly aged controls. Investigators decided a priori that if vaginal and/or urinary microbiomes differed between continent and incontinent women, the groups would be analyzed separately; if similar, samples from continent and incontinent women would be pooled and analyzed together. A central laboratory sequenced variable regions 1-3 (v1-3) and characterized bacteria to the genus level. Operational taxonomic unit abundance was described for paired vaginal and urine samples. Pearson's correlation characterized the relationship between individual operational taxonomic units of paired samples. Canonical correlation analysis evaluated the association between clinical variables (including mixed urinary incontinence and control status) and vaginal and urinary operational taxonomic units, using the Canonical correlation analysis function in the Vegan package (R version 3.5). Linear discriminant analysis effect size was used to find taxa that discriminated between vaginal and urinary samples.ResultsUrinary and vaginal samples were collected from 212 women (mean age 53±11 years) and results from 197 paired samples were available for analysis. As operational taxonomic units in mixed urinary incontinence and control samples were related in canonical correlation analysis and since taxa did not discriminate between mixed urinary incontinence or controls in either vagina or urine, mixed urinary incontinence and control samples were pooled for further analysis. Canonical correlation analysis of vaginal and urinary samples indicated that that 60 of the 100 most abundant operational taxonomic units in the samples largely overlapped. Lactobacillus was the most abundant genus in both urine and vagina (contributing on average 53% to an individual's urine sample and 64% to an individual's vaginal sample) (Pearson correlation r=0.53). Although less abundant than Lactobacillus, other bacteria with high Pearson correlation coefficients also commonly found in vagina and urine included: Gardnerella (r=0.70), Prevotella (r=0.64), and Ureaplasma (r=0.50). Linear discriminant analysis effect size analysis identified Tepidimonas and Flavobacterium as bacteria that distinguished the urinary environment for both mixed urinary incontinence and controls as these bacteria were absent in the vagina (Tepidimonas effect size 2.38, P<.001, Flavobacterium effect size 2.15, P<.001). Although Lactobacillus was the most abundant bacteria in both urine and vagina, it was more abundant in the vagina (linear discriminant analysis effect size effect size 2.72, P<.001).ConclusionSignificant associations between vaginal and urinary microbiomes were demonstrated, with Lactobacillus being predominant in both urine and vagina. Abundance of other bacteria also correlated highly between the vagina and urine. This inter-relatedness has implications for studying manipulation of the urogenital microbiome in treating conditions such as urgency urinary incontinence and urinary tract infections.

Project description:ObjectivesTo examine the influence of sexual activity on the composition and consistency of the vaginal microbiota over time, and distribution of Gardnerella vaginalis clades in young women.MethodsFifty-two participants from a university cohort were selected. Vaginal swabs were self-collected every 3-months for up to 12 months with 184 specimens analysed. The vaginal microbiota was characterised using Roche 454 V3/4 region 16S rRNA sequencing, and G.vaginalis clade typing by qPCR.ResultsA Lactobacillus crispatus dominated vaginal microbiota was associated with Caucasian ethnicity (adjusted relative risk ratio[ARRR] = 7.28, 95%CI:1.37,38.57,p = 0.020). An L.iners (ARRR = 17.51, 95%CI:2.18,140.33,p = 0.007) or G.vaginalis (ARRR = 14.03, 95%CI:1.22,160.69, p = 0.034) dominated microbiota was associated with engaging in penile-vaginal sex. Microbiota dominated by L.crispatus, L.iners or other lactobacilli exhibited greater longitudinal consistency of the bacterial communities present compared to ones dominated by heterogeneous non-lactobacilli (p<0.030); sexual activity did not influence consistency. Women who developed BV were more likely to have clade GV4 compared to those reporting no sex/practiced non-coital activities (OR = 11.82, 95%CI:1.87,74.82,p = 0.009). Specimens were more likely to contain multiple G.vaginalis clades rather than a single clade if women engaged in penile-vaginal sex (RRR = 9.55, 95%CI:1.33,68.38,p = 0.025) or were diagnosed with BV (RRR = 31.5, 95%CI:1.69,586.87,p = 0.021).ConclusionsSexual activity and ethnicity influenced the composition of the vaginal microbiota of these young, relatively sexually inexperienced women. Women had consistent vaginal microbiota over time if lactobacilli were the dominant spp. present. Penile-vaginal sex did not alter the consistency of microbial communities but increased G.vaginalis clade diversity in young women with and without BV, suggesting sexual transmission of commensal and potentially pathogenic clades.

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Genome Investigation of Urinary Gardnerella Strains and Their Relationship to Isolates of the Vaginal Microbiota.

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