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Competition Among Gardnerella Subgroups From the Human Vaginal Microbiome.

ABSTRACT: Gardnerella spp. are hallmarks of bacterial vaginosis, a clinically significant dysbiosis of the vaginal microbiome. Gardnerella has four subgroups (A, B, C, and D) based on cpn60 sequences. Multiple subgroups are often detected in individual women, and interactions between these subgroups are expected to influence their population dynamics and associated clinical signs and symptoms of bacterial vaginosis. In the present study, contact-independent and contact-dependent interactions between the four Gardnerella subgroups were investigated in vitro. The cell free supernatants of mono- and co-cultures had no effect on growth rates of the Gardnerella subgroups suggesting that there are no contact-independent interactions (and no contest competition). For contact-dependent interactions, mixed communities of 2, 3, or 4 subgroups were created and the initial (0 h) and final population sizes (48 h) were quantified using subgroup-specific PCR. Compared to the null hypothesis of neutral interactions, most (69.3%) of the mixed communities exhibited competition. Competition reduced the growth rates of subgroups A, B, and C. In contrast, the growth rate of subgroup D increased in the presence of the other subgroups. All subgroups were able to form biofilm alone and in mixed communities. Our study suggests that there is scramble competition among Gardnerella subgroups, which likely contributes to the observed distributions of Gardnerella spp. in vaginal microbiomes and the formation of the multispecies biofilms characteristic of bacterial vaginosis.

SUBMITTER: Khan S

PROVIDER: S-EPMC6834547 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Competition Among Gardnerella Subgroups From the Human Vaginal Microbiome.

Khan Salahuddin S Voordouw Maarten J MJ Hill Janet E JE

Frontiers in cellular and infection microbiology 20191031

Gardnerella spp. are hallmarks of bacterial vaginosis, a clinically significant dysbiosis of the vaginal microbiome. Gardnerella has four subgroups (A, B, C, and D) based on cpn60 sequences. Multiple subgroups are often detected in individual women, and interactions between these subgroups are expected to influence their population dynamics and associated clinical signs and symptoms of bacterial vaginosis. In the present study, contact-independent and contact-dependent interactions ...[more]

PMID: 31737577

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Project description:Multiple Gardnerella species frequently cooccur in vaginal microbiomes, and several factors, including competition for nutrients such as glycogen could determine their population structure. Although Gardnerella spp. can hydrolyze glycogen to produce glucose, maltose, maltotriose, and maltotetraose, how these sugars are transported and utilized for growth is unknown. We determined the distribution of genes encoding transporter proteins associated with the uptake of glucose, maltose, and malto-oligosaccharides and maltodextrins among Gardnerella species. A total of five different ABC transporters were identified in Gardnerella spp. of which MusEFGK2I and MalXFGK were conserved across all 15 Gardnerella isolates. RafEFGK and TMSP (trehalose, maltose, sucrose, and palatinose) operons were specific to G. vaginalis while the MalEFG transporter was identified in G. leopoldii only. Although no glucose specific sugar-symporters were identified, putative "glucose/galactose porters" and components of a phosphotransferase system were identified. In laboratory experiments, all Gardnerella isolates grew more in the presence of glucose, maltose, maltotriose, and maltotetraose compared to unsupplemented media. In addition, most isolates (10/15) showed significantly more growth on maltotetraose compared to glucose (Kruskal Wallis, P < 0.05) suggesting their preference for longer chain malto-oligosaccharides. Our findings show that although putative MusEFGK2I and MalXFGK transporters are found in all Gardnerella spp., some species-specific transporters are also present. Observed distribution of genes encoding transporter systems was consistent with laboratory observations that Gardnerella spp. grow better on longer chain malto-oligosaccharides. IMPORTANCE Increased abundance of Gardnerella spp. is a diagnostic characteristic of bacterial vaginosis, an imbalance in the human vaginal microbiome associated with troubling symptoms and negative reproductive health outcomes, including increased transmission of sexually transmitted infections and preterm birth. Competition for nutrients is likely an important factor in causing dramatic shifts in the vaginal microbial community. Gardnerella produces enzymes to digest glycogen, an important nutrient source for vaginal bacteria, but little is known about the mechanisms in Gardnerella for uptake of the products of this digestion, or whether Gardnerella use some or all of the products. Our results indicate that Gardnerella may have evolved to preferentially use a subset of the glycogen breakdown products, which would help them reduce direct competition with some other bacteria in the vagina.

Project description:Gardnerella spp. in the vaginal microbiome are associated with bacterial vaginosis, in which a lactobacillus-dominated community is replaced with mixed bacteria, including Gardnerella species. Co-occurrence of multiple Gardnerella species in the vaginal environment is common, but different species are dominant in different women. Competition for nutrients, including glycogen, could play an important role in determining the microbial community structure. Digestion of glycogen into products that can be taken up and further processed by bacteria requires the combined activities of several enzymes collectively known as amylases, which belong to glycoside hydrolase family 13 (GH13) within the CAZy classification system. GH13 is a large and diverse family of proteins, making prediction of their activities challenging. SACCHARIS annotation of the GH13 family in Gardnerella resulted in identification of protein domains belonging to eight subfamilies. Phylogenetic analysis of predicted amylase sequences from 26 genomes demonstrated that a putative α-glucosidase-encoding sequence, CG400_06090, was conserved in all Gardnerella spp. The predicted α-glucosidase enzyme was expressed, purified, and functionally characterized. The enzyme was active on a variety of maltooligosaccharides with maximum activity at pH 7. Km, kcat, and kcat/Km values for the substrate 4-nitrophenyl α-d-glucopyranoside were 8.3 μM, 0.96 min-1, and 0.11 μM-1 min-1, respectively. Glucose was released from maltose, maltotriose, maltotetraose, and maltopentaose, but no products were detected when the enzyme was incubated with glycogen. Our findings show that Gardnerella spp. produce an α-glucosidase enzyme that may contribute to the multistep process of glycogen metabolism by releasing glucose from maltooligosaccharides. IMPORTANCE Increased abundance of Gardnerella spp. is a diagnostic characteristic of bacterial vaginosis, an imbalance in the human vaginal microbiome associated with troubling symptoms, and negative reproductive health outcomes, including increased transmission of sexually transmitted infections and preterm birth. Competition for nutrients is likely an important factor in causing dramatic shifts in the vaginal microbial community but little is known about the contribution of bacterial enzymes to the metabolism of glycogen, a major carbon source available to vaginal bacteria. The significance of our research is characterizing the activity of an enzyme conserved in Gardnerella species that likely contributes to the ability of these bacteria to utilize glycogen.

Dataset Information

Competition Among Gardnerella Subgroups From the Human Vaginal Microbiome.

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Competition Among <i>Gardnerella</i> Subgroups From the Human Vaginal Microbiome.

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