Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the Vagina
Glycogen in the female lower reproductive tract is a major carbon source for colonization and acidification by common vaginal <i>Lactobacillus</i> species, such as <i>Lactobacillus crispatus</i>. Previously, we identified the amylopullulanase encoding gene <i>pulA</i...
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| Format: | Article |
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MDPI AG
2022-05-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/10/5590 |
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| author | Rosanne Hertzberger Ali May Gertjan Kramer Isabelle van Vondelen Douwe Molenaar Remco Kort |
| author_facet | Rosanne Hertzberger Ali May Gertjan Kramer Isabelle van Vondelen Douwe Molenaar Remco Kort |
| author_sort | Rosanne Hertzberger |
| collection | DOAJ |
| description | Glycogen in the female lower reproductive tract is a major carbon source for colonization and acidification by common vaginal <i>Lactobacillus</i> species, such as <i>Lactobacillus crispatus</i>. Previously, we identified the amylopullulanase encoding gene <i>pulA</i> of <i>Lactobacillus crispatus</i> to correlate with the ability to autonomously utilize glycogen for growth. Here, we further characterize genetic variation and differential regulation of <i>pulA</i> affecting the presence of its gene product on the outer surface layer. We show that alpha-glucan degrading activity dissipates when <i>Lactobacillus crispatus</i> is grown on glucose, maltose and maltotriose, in agreement with carbon catabolite repression elements flanking the <i>pulA</i> gene. Proteome analysis of the S-layer confirmed that the amylopullulanase protein is highly abundant in an S-layer enriched fraction, but not in a strain with a defective amylopullulanase variant or in an amylopullulanase-sufficient strain grown on glucose. In addition, we provide evidence that <i>Lactobacillus crispatus pulA</i> mutants are relevant in vivo, as they are commonly observed in metagenome datasets of human vaginal microbial communities. Analysis of the largest publicly available dataset of 1507 human vaginal metagenomes indicates that among the 270 samples that contain a <i>Lactobacillus crispatus</i><i>pulA</i> gene, 62 samples (23%) had a defective variant of this gene. Taken together, these results demonstrate that both environmental, as well as genetic factors explain the variation of <i>Lactobacillus crispatus</i> alpha-glucosidases in the vaginal environment. |
| first_indexed | 2024-03-10T03:44:24Z |
| format | Article |
| id | doaj.art-609b7c55c2834f1692ed90dddf60a787 |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T03:44:24Z |
| publishDate | 2022-05-01 |
| publisher | MDPI AG |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-609b7c55c2834f1692ed90dddf60a7872023-11-23T11:25:08ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-05-012310559010.3390/ijms23105590Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the VaginaRosanne Hertzberger0Ali May1Gertjan Kramer2Isabelle van Vondelen3Douwe Molenaar4Remco Kort5Department of Molecular Cell Biology, Vrije Universiteit Amsterdam, De Boelelaan 1108, 1081 HZ Amsterdam, The NetherlandsARTIS-Micropia, Plantage Kerklaan 38-40, 1018 CZ Amsterdam, The NetherlandsLaboratory for Mass Spectrometry of Biomolecules, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The NetherlandsDepartment of Molecular Cell Biology, Vrije Universiteit Amsterdam, De Boelelaan 1108, 1081 HZ Amsterdam, The NetherlandsDepartment of Molecular Cell Biology, Vrije Universiteit Amsterdam, De Boelelaan 1108, 1081 HZ Amsterdam, The NetherlandsDepartment of Molecular Cell Biology, Vrije Universiteit Amsterdam, De Boelelaan 1108, 1081 HZ Amsterdam, The NetherlandsGlycogen in the female lower reproductive tract is a major carbon source for colonization and acidification by common vaginal <i>Lactobacillus</i> species, such as <i>Lactobacillus crispatus</i>. Previously, we identified the amylopullulanase encoding gene <i>pulA</i> of <i>Lactobacillus crispatus</i> to correlate with the ability to autonomously utilize glycogen for growth. Here, we further characterize genetic variation and differential regulation of <i>pulA</i> affecting the presence of its gene product on the outer surface layer. We show that alpha-glucan degrading activity dissipates when <i>Lactobacillus crispatus</i> is grown on glucose, maltose and maltotriose, in agreement with carbon catabolite repression elements flanking the <i>pulA</i> gene. Proteome analysis of the S-layer confirmed that the amylopullulanase protein is highly abundant in an S-layer enriched fraction, but not in a strain with a defective amylopullulanase variant or in an amylopullulanase-sufficient strain grown on glucose. In addition, we provide evidence that <i>Lactobacillus crispatus pulA</i> mutants are relevant in vivo, as they are commonly observed in metagenome datasets of human vaginal microbial communities. Analysis of the largest publicly available dataset of 1507 human vaginal metagenomes indicates that among the 270 samples that contain a <i>Lactobacillus crispatus</i><i>pulA</i> gene, 62 samples (23%) had a defective variant of this gene. Taken together, these results demonstrate that both environmental, as well as genetic factors explain the variation of <i>Lactobacillus crispatus</i> alpha-glucosidases in the vaginal environment.https://www.mdpi.com/1422-0067/23/10/5590<i>Lactobacillus crispatus</i>amylopullulanaseglycogen |
| spellingShingle | Rosanne Hertzberger Ali May Gertjan Kramer Isabelle van Vondelen Douwe Molenaar Remco Kort Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the Vagina International Journal of Molecular Sciences <i>Lactobacillus crispatus</i> amylopullulanase glycogen |
| title | Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the Vagina |
| title_full | Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the Vagina |
| title_fullStr | Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the Vagina |
| title_full_unstemmed | Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the Vagina |
| title_short | Genetic Elements Orchestrating <i>Lactobacillus crispatus</i> Glycogen Metabolism in the Vagina |
| title_sort | genetic elements orchestrating i lactobacillus crispatus i glycogen metabolism in the vagina |
| topic | <i>Lactobacillus crispatus</i> amylopullulanase glycogen |
| url | https://www.mdpi.com/1422-0067/23/10/5590 |
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