Bacterial amylases enable glycogen degradation by the vaginal microbiome

Jenkins, Dominick J.; Woolston, Benjamin M.; Hood-Pishchany, M. Indriati; Pelayo, Paula; Konopaski, Alyssa N.; Quinn Peters, M.; France, Michael T.; Ravel, Jacques; Mitchell, Caroline M.; Rakoff-Nahoum, Seth; Whidbey, Christopher; Balskus, Emily P.

doi:10.1038/s41564-023-01447-2

Cited by 15 publications

(4 citation statements)

References 67 publications

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“…have been shown to directly use glycogen for growth (71,72). Here we show that P. timonensis, G. vaginalis, and P. bivia were all able to grow on glycogen as single nutrient source, which is in line with the presence of α-glucosidases in their genomes (25,50). Overall, glycogen utilization seems to be a shared trait of vagina-associated bacteria, indicating their adaptation to the vaginal environment.…”

Section: Discussionsupporting

confidence: 71%

“…Vaginal and cervical epithelial cells produce high amounts of glycogen, which is deposited onto the epithelium once epithelial cells are shed and lysed (48,49) and can serve as a carbon source for the resident vaginal bacteria (50). We investigated whether our selected BV-associated bacteria could utilize glycogen for growth.…”

Section: Utilization Of Glycogen and Mucins As Carbon Sources By Bv-a...mentioning

confidence: 99%

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Prevotella timonensisdegrades the vaginal epithelial glycocalyx through high fucosidase and sialidase activities

Segui-Perez,

de Jongh,

Jonkergouw

et al. 2024

Preprint

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Bacterial vaginosis (BV) is a polymicrobial infection of the female reproductive tract (FRT). BV is characterized by replacement of health-associatedLactobacillusspecies by diverse anaerobic bacteria, including the well-knownGardnerella vaginalis.Prevotella timonensisandPrevotella biviaare anaerobes that are found in a significant percentage of BV patients, but their pathogenic properties are yet to be determined. Defining characteristics of anaerobic overgrowth in BV are adherence to the mucosal surface and the increased activity of mucin-degrading enzymes such as sialidases in vaginal secretions. Here, we demonstrate thatP. timonensisbut notP. biviastrongly adhered to vaginal and endocervical cells to a similar level asG. vaginalisbut did not elicit a comparable pro-inflammatory response. TheP. timonensisgenome uniquely encodes a large set of mucus-degrading enzymes including 4 putative fucosidases and 2 putative sialidases, PtNanH1 and PtNanH2. Enzyme assays demonstrated that fucosidase and sialidase activity inP. timonensiscell-bound and secreted fractions was significantly higher than for other vaginal anaerobes. Infection assays revealed thatP. timonensisfucosidases and sialidases efficiently removed fucose and α2,3- and α2,6-linked sialic acid moieties from the epithelial glycocalyx. Recombinantly expressedP. timonensisNanH1 and NanH2 efficiently removed α2,3 and α2,6-linked sialic acids from the epithelial surface and sialic acid removal byP. timonensiscould be blocked using inhibitors. This study demonstrates thatP.timonensishas distinct virulence properties that include initial adhesion and a high capacity for mucin degradation at the vaginal epithelial mucosal surface. Our results underline the importance of understanding the role of different anaerobic bacteria in BV.Significance statement (Layman)Bacterial vaginosis (BV) is a common vaginal infection that affects a high percentage of women and is associated with reduced fertility and increased risk of secondary infections.Gardnerella vaginalisis the most well-known BV-associated bacterium, butPrevotellaspecies includingP. timonensisandP. biviamay also play an important role. We showed that, similar toG. vaginalis,P. timonensisadhered well to the vaginal epithelium, suggesting that both bacteria could be important in the first stage of infection. Compared to the other bacteria,P. timonensiswas unique in efficiently removing the protective mucin sugars that cover the vaginal epithelium. These results underscore that vaginal bacteria play different roles in the initiation and development of BV.

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Section: Discussionsupporting

confidence: 71%

Section: Utilization Of Glycogen and Mucins As Carbon Sources By Bv-a...mentioning

confidence: 99%

Prevotella timonensisdegrades the vaginal epithelial glycocalyx through high fucosidase and sialidase activities

Segui-Perez,

de Jongh,

Jonkergouw

et al. 2024

Preprint

Self Cite

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“…In the research setting, they have been used for the study of cells present in menstrual blood ( 30 , 31 ). In addition, they can be used to collect CVF in individuals while not menstruating ( 32 – 34 ). For example, menstrual discs have been used previously for the study of cytokines and other soluble markers in CVF ( 34 – 36 ).…”

Section: Introductionmentioning

confidence: 99%

A Noninvasive Method to Sample Immune Cells in the Lower Female Genital Tract Using Menstrual Discs

Peters,

Domenjo-Vila,

Carlson

et al. 2024

ImmunoHorizons

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T cells in the human female genital tract (FGT) are key mediators of susceptibility to and protection from infection, including HIV and other sexually transmitted infections. There is a critical need for increased understanding of the distribution and activation of T cell populations in the FGT, but current sampling methods require a healthcare provider and are expensive, limiting the ability to study these populations longitudinally. To address these challenges, we have developed a method to sample immune cells from the FGT utilizing disposable menstrual discs which are noninvasive, self-applied, and low in cost. To demonstrate reproducibility, we sampled the cervicovaginal fluid of healthy, reproductive-aged individuals using menstrual discs across 3 sequential days. Cervicovaginal fluid was processed for cervicovaginal cells, and high-parameter flow cytometry was used to characterize immune populations. We identified large numbers of live, CD45+ leukocytes, as well as distinct populations of T cells and B cells. Within the T cell compartment, activation and suppression status of T cell subsets were consistent with previous studies of the FGT utilizing current approaches, including identification of both tissue-resident and migratory populations. In addition, the T cell population structure was highly conserved across days within individuals but divergent across individuals. Our approach to sample immune cells in the FGT with menstrual discs will decrease barriers to participation and empower longitudinal sampling in future research studies.

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“…In the research setting, they have been used for the study of cells present in menstrual blood (30, 31). In addition, they can be used to collect CVF in individuals while not menstruating (32–34) ( Figure 1A , B ). For example, menstrual discs have been used previously for the study of cytokines and other soluble markers in CVF (34–36).…”

Section: Introductionmentioning

confidence: 99%

A non-invasive method to sample immune cells in the lower female genital tract using menstrual discs

Quinn Peters,

Domenjo-Vila,

Carlson

et al. 2023

Preprint

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T cells in the female genital tract (FGT) are a key mediator of susceptibility to and protection from infection, including HIV and other sexually transmitted infections. There is a critical need for increased understanding of the distribution and activation of T cell populations in the FGT, but current sampling methods are invasive and expensive, limiting the ability to study these populations longitudinally. To address these challenges, we have developed a novel method to sample immune cells from the FGT utilizing disposable menstrual discs which are non-invasive, self-applied, and low-cost. To demonstrate reproducibility, we sampled the cervicovaginal fluid (CVF) of healthy, reproductive-aged individuals using menstrual discs over three sequential days. CVF was processed for cervicovaginal cells, and high parameter flow cytometry was used to characterize immune populations. We identified large numbers of live, CD45+ leukocytes, as well as populations of T cells and B cells. Within the T cell compartment, phenotypic features of T cell subsets were consistent with previous FGT studies utilizing more invasive approaches, including identification of both tissue resident and migratory populations. In addition, the T cell population structure was highly reproducible across days within individuals but divergent across individuals. Our novel approach to sampling immune cells in the FGT will decrease barriers to participation and empower longitudinal sampling in future research studies.

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Bacterial amylases enable glycogen degradation by the vaginal microbiome

Cited by 15 publications

References 67 publications

Prevotella timonensisdegrades the vaginal epithelial glycocalyx through high fucosidase and sialidase activities

Prevotella timonensisdegrades the vaginal epithelial glycocalyx through high fucosidase and sialidase activities

A Noninvasive Method to Sample Immune Cells in the Lower Female Genital Tract Using Menstrual Discs

A non-invasive method to sample immune cells in the lower female genital tract using menstrual discs

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