Transport and utilization of glycogen breakdown products by<i>Gardnerella</i>spp. from the human vaginal microbiome

Bhandari, Pashupati; Hill, Janet E.

doi:10.1101/2022.11.01.514706

Cited by 2 publications

(3 citation statements)

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“…The larger breakdown products of glycogen digestion (maltose, maltotriose, maltotetraose, malto-oligosaccharides) and extracellular glucose are taken up by two distinct types of transport systems. Products of glycogen digestion are transported into lactobacilli through the four component ATP-binding cassette transport system MalEFG/MsmK [ 73 , 74 ] while G. vaginalis has four separate transport systems for these products: the MusEFGK2I operon (maltose/maltotriose), the MalXFGK transporter (maltose, maltotriose, malto-oligosaccharides and maltodextrins), RafEFGK (α-1,6 linked glucosides and galactosides), and TMSP 322 (trehalose/maltose) [ 75 ]. Similar to E. coli and other bacteria, glucose can be transported into L. jensenii , L. gasseri and L. crispatus by the phosphoenolpyruvate: carbohydrate phosphotransferase system [ 76 , 77 ] and into G. vaginalis by a putative glucose/galactose porter [ 75 ].…”

Section: Discussionmentioning

confidence: 99%

“…Products of glycogen digestion are transported into lactobacilli through the four component ATP-binding cassette transport system MalEFG/MsmK [ 73 , 74 ] while G. vaginalis has four separate transport systems for these products: the MusEFGK2I operon (maltose/maltotriose), the MalXFGK transporter (maltose, maltotriose, malto-oligosaccharides and maltodextrins), RafEFGK (α-1,6 linked glucosides and galactosides), and TMSP 322 (trehalose/maltose) [ 75 ]. Similar to E. coli and other bacteria, glucose can be transported into L. jensenii , L. gasseri and L. crispatus by the phosphoenolpyruvate: carbohydrate phosphotransferase system [ 76 , 77 ] and into G. vaginalis by a putative glucose/galactose porter [ 75 ]. As with the glycogen utilization proteins, i n silico analysis revealed presence of transportation systems for glycogen breakdown products in our tested strains (Table S2 ).…”

Section: Discussionmentioning

confidence: 99%

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Glycogen availability and pH variation in a medium simulating vaginal fluid influence the growth of vaginal Lactobacillus species and Gardnerella vaginalis

et al. 2023

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Background Glycogen metabolism by Lactobacillus spp. that dominate the healthy vaginal microbiome contributes to a low vaginal pH (3.5–4.5). During bacterial vaginosis (BV), strict and facultative anaerobes including Gardnerella vaginalis become predominant, leading to an increase in the vaginal pH (> 4.5). BV enhances the risk of obstetrical complications, acquisition of sexually transmitted infections, and cervical cancer. Factors critical for the maintenance of the healthy vaginal microbiome or the transition to the BV microbiome are not well defined. Vaginal pH may affect glycogen metabolism by the vaginal microflora, thus influencing the shift in the vaginal microbiome. Results The medium simulating vaginal fluid (MSVF) supported growth of L. jensenii 62G, L. gasseri 63 AM, and L. crispatus JV-V01, and G. vaginalis JCP8151A at specific initial pH conditions for 30 d. L. jensenii at all three starting pH levels (pH 4.0, 4.5, and 5.0), G. vaginalis at pH 4.5 and 5.0, and L. gasseri at pH 5.0 exhibited the long-term stationary phase when grown in MSVF. L. gasseri at pH 4.5 and L. crispatus at pH 5.0 displayed an extended lag phase over 30 d suggesting inefficient glycogen metabolism. Glycogen was essential for the growth of L. jensenii, L. crispatus, and G. vaginalis; only L. gasseri was able to survive in MSVF without glycogen, and only at pH 5.0, where it used glucose. All four species were able to survive for 15 d in MSVF with half the glycogen content but only at specific starting pH levels – pH 4.5 and 5.0 for L. jensenii, L. gasseri, and G. vaginalis and pH 5.0 for L. crispatus. Conclusions These results suggest that variations in the vaginal pH critically influence the colonization of the vaginal tract by lactobacilli and G. vaginalis JCP8151A by affecting their ability to metabolize glycogen. Further, we found that L. jensenii 62G is capable of glycogen metabolism over a broader pH range (4.0–5.0) while L. crispatus JV-V01 glycogen utilization is pH sensitive (only functional at pH 5.0). Finally, our results showed that G. vaginalis JCP8151A can colonize the vaginal tract for an extended period as long as the pH remains at 4.5 or above.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Glycogen availability and pH variation in a medium simulating vaginal fluid influence the growth of vaginal Lactobacillus species and Gardnerella vaginalis

et al. 2023

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“…A heterologously expressed homologue of this enzyme in Gardnerella was found to degrade amylose, pullulan, glycogen and starch (23). Recent research showed that 14 out of 15 tested Gardnerella strains carried a full copy of this gene (17) and that isolates of four different Gardnerella species can transport and metabolize the small maltodextrins derived from glycogen breakdown (24).…”

Section: Introductionmentioning

confidence: 99%

Bacterial vaginosis is associated with increased amylolytic activity

Hertzberger

Himschoot

Bruisten

et al. 2023

Preprint

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Glycogen is the most abundant vaginal carbohydrate in reproductive aged women. Reduced vaginal glycogen is associated with lower levels of Lactobacillus crispatus, overgrowth of fastidious anaerobes such as Gardnerella vaginalis and increased risk of adverse reproductive and sexual health outcomes. Here we show that Gardnerella vaginalis, Lactobacillus iners and Lactobacillus crispatus can autonomously utilize glycogen as a source for growth. Using an ungelatinized and labeled form of raw amylose, a more degradation-resistant α-1,4-glucan, we were able to discriminate between the alpha-glucosidase activities of common vaginal bacterial species. The bacteria Lactobacillus crispatus, Lactobacillus iners, Gardnerella piotii as well as several other common vaginal species were not capable of raw amylose degradation, while Gardnerella vaginalis, Gardnerella swidsinskii and Gardnerella leopoldii were, with the latter two having the highest degradation rates. In contrast to the glycogen-degrading activity we previously identified in Lactobacillus crispatus, this Gardnerella alpha-glucosidase activity was not cell-bound and not repressed in the presence of glucose. Raw amylose degradation activity in vaginal swabs was strongly associated with bacterial vaginosis as assessed by Nugent scoring. Overall, our results show that the dysbiotic microbiota of bacterial vaginosis is associated with increased amylolytic activity, which is also found in pure cultures of Gardnerella species, but not in other common vaginal bacteria.

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Transport and utilization of glycogen breakdown products byGardnerellaspp. from the human vaginal microbiome

Cited by 2 publications

References 38 publications

Glycogen availability and pH variation in a medium simulating vaginal fluid influence the growth of vaginal Lactobacillus species and Gardnerella vaginalis

Glycogen availability and pH variation in a medium simulating vaginal fluid influence the growth of vaginal Lactobacillus species and Gardnerella vaginalis

Bacterial vaginosis is associated with increased amylolytic activity

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