The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae.
Vibrio cholerae is a facultative pathogen that primarily occupies marine environments. In this niche, V. cholerae commonly interacts with the chitinous shells of crustacean zooplankton. As a chitinolytic microbe, V. cholerae degrades insoluble chitin into soluble oligosaccharides. Chitin oligosaccha...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2023-05-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1010767 |
| _version_ | 1797682819017736192 |
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| author | Virginia E Green Catherine A Klancher Shouji Yamamoto Ankur B Dalia |
| author_facet | Virginia E Green Catherine A Klancher Shouji Yamamoto Ankur B Dalia |
| author_sort | Virginia E Green |
| collection | DOAJ |
| description | Vibrio cholerae is a facultative pathogen that primarily occupies marine environments. In this niche, V. cholerae commonly interacts with the chitinous shells of crustacean zooplankton. As a chitinolytic microbe, V. cholerae degrades insoluble chitin into soluble oligosaccharides. Chitin oligosaccharides serve as both a nutrient source and an environmental cue that induces a strong transcriptional response in V. cholerae. Namely, these oligosaccharides induce the chitin sensor, ChiS, to activate the genes required for chitin utilization and horizontal gene transfer by natural transformation. Thus, interactions with chitin impact the survival of V. cholerae in marine environments. Chitin is a complex carbon source for V. cholerae to degrade and consume, and the presence of more energetically favorable carbon sources can inhibit chitin utilization. This phenomenon, known as carbon catabolite repression (CCR), is mediated by the glucose-specific Enzyme IIA (EIIAGlc) of the phosphoenolpyruvate-dependent phosphotransferase system (PTS). In the presence of glucose, EIIAGlc becomes dephosphorylated, which inhibits ChiS transcriptional activity by an unknown mechanism. Here, we show that dephosphorylated EIIAGlc interacts with ChiS. We also isolate ChiS suppressor mutants that evade EIIAGlc-dependent repression and demonstrate that these alleles no longer interact with EIIAGlc. These findings suggest that EIIAGlc must interact with ChiS to exert its repressive effect. Importantly, the ChiS suppressor mutations we isolated also relieve repression of chitin utilization and natural transformation by EIIAGlc, suggesting that CCR of these behaviors is primarily regulated through ChiS. Together, our results reveal how nutrient conditions impact the fitness of an important human pathogen in its environmental reservoir. |
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| id | doaj.art-96da2d807b254e4c840226d811fdb4d7 |
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| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-03-12T00:05:21Z |
| publishDate | 2023-05-01 |
| publisher | Public Library of Science (PLoS) |
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| series | PLoS Genetics |
| spelling | doaj.art-96da2d807b254e4c840226d811fdb4d72023-09-17T05:30:54ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-05-01195e101076710.1371/journal.pgen.1010767The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae.Virginia E GreenCatherine A KlancherShouji YamamotoAnkur B DaliaVibrio cholerae is a facultative pathogen that primarily occupies marine environments. In this niche, V. cholerae commonly interacts with the chitinous shells of crustacean zooplankton. As a chitinolytic microbe, V. cholerae degrades insoluble chitin into soluble oligosaccharides. Chitin oligosaccharides serve as both a nutrient source and an environmental cue that induces a strong transcriptional response in V. cholerae. Namely, these oligosaccharides induce the chitin sensor, ChiS, to activate the genes required for chitin utilization and horizontal gene transfer by natural transformation. Thus, interactions with chitin impact the survival of V. cholerae in marine environments. Chitin is a complex carbon source for V. cholerae to degrade and consume, and the presence of more energetically favorable carbon sources can inhibit chitin utilization. This phenomenon, known as carbon catabolite repression (CCR), is mediated by the glucose-specific Enzyme IIA (EIIAGlc) of the phosphoenolpyruvate-dependent phosphotransferase system (PTS). In the presence of glucose, EIIAGlc becomes dephosphorylated, which inhibits ChiS transcriptional activity by an unknown mechanism. Here, we show that dephosphorylated EIIAGlc interacts with ChiS. We also isolate ChiS suppressor mutants that evade EIIAGlc-dependent repression and demonstrate that these alleles no longer interact with EIIAGlc. These findings suggest that EIIAGlc must interact with ChiS to exert its repressive effect. Importantly, the ChiS suppressor mutations we isolated also relieve repression of chitin utilization and natural transformation by EIIAGlc, suggesting that CCR of these behaviors is primarily regulated through ChiS. Together, our results reveal how nutrient conditions impact the fitness of an important human pathogen in its environmental reservoir.https://doi.org/10.1371/journal.pgen.1010767 |
| spellingShingle | Virginia E Green Catherine A Klancher Shouji Yamamoto Ankur B Dalia The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae. PLoS Genetics |
| title | The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae. |
| title_full | The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae. |
| title_fullStr | The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae. |
| title_full_unstemmed | The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae. |
| title_short | The molecular mechanism for carbon catabolite repression of the chitin response in Vibrio cholerae. |
| title_sort | molecular mechanism for carbon catabolite repression of the chitin response in vibrio cholerae |
| url | https://doi.org/10.1371/journal.pgen.1010767 |
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