Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae
Abstract The replication of the two chromosomes in the pathogenic bacterium Vibrio cholerae is coordinated by the binding of initiator protein RctB to a checkpoint sequence, crtS. Replication of crtS on the primary chromosome (Chr1) triggers replication of the secondary chromosome (Chr2), but the de...
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Nature Portfolio
2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55598-9 |
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| author | Théophile Niault Ariel Talavera Eric Le Cam Sonia Baconnais Ole Skovgaard Florian Fournes Léa Wagner Hedvig Tamman Andrew Thompson Dannele Echemendia-Blanco Noa Guzzi Abel Garcia-Pino Didier Mazel Marie-Eve Val |
| author_facet | Théophile Niault Ariel Talavera Eric Le Cam Sonia Baconnais Ole Skovgaard Florian Fournes Léa Wagner Hedvig Tamman Andrew Thompson Dannele Echemendia-Blanco Noa Guzzi Abel Garcia-Pino Didier Mazel Marie-Eve Val |
| author_sort | Théophile Niault |
| collection | DOAJ |
| description | Abstract The replication of the two chromosomes in the pathogenic bacterium Vibrio cholerae is coordinated by the binding of initiator protein RctB to a checkpoint sequence, crtS. Replication of crtS on the primary chromosome (Chr1) triggers replication of the secondary chromosome (Chr2), but the details are poorly understood. Here, we analyze RctB binding patterns in the V. cholerae genome across various cell cycle stages. We find that RctB primarily binds to sites inhibiting replication initiation at the Chr2 origin (ori2). This inhibitory effect is counteracted when crtS is replicated on Chr1, causing a shift in RctB binding to sites that activate replication at ori2. Structural analyzes indicate the formation of diverse oligomeric states of RctB, coupled to the allosteric effect of DNA, which determine ori2 accessibility. We propose a synchronization model where, upon replication, crtS locally destabilizes the RctB inhibition complex, releasing the Chr2 replication origin. |
| format | Article |
| id | doaj-art-ce89768fa52243a4a2040fe3aff0d406 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-ce89768fa52243a4a2040fe3aff0d4062025-01-12T12:30:34ZengNature PortfolioNature Communications2041-17232025-01-0116111610.1038/s41467-024-55598-9Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio choleraeThéophile Niault0Ariel Talavera1Eric Le Cam2Sonia Baconnais3Ole Skovgaard4Florian Fournes5Léa Wagner6Hedvig Tamman7Andrew Thompson8Dannele Echemendia-Blanco9Noa Guzzi10Abel Garcia-Pino11Didier Mazel12Marie-Eve Val13Institut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien, Département Génomes et GénétiqueCellular and Molecular Microbiology, Faculté des Sciences, Université libre de Bruxelles (ULB), Boulevard du TriompheGenome Integrity and Cancer UMR 9019 CNRS, Université Paris Saclay, Gustave RoussyGenome Integrity and Cancer UMR 9019 CNRS, Université Paris Saclay, Gustave RoussyDepartment of Science and Environment, Systems and Models, Roskilde UniversityInstitut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien, Département Génomes et GénétiqueInstitut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien, Département Génomes et GénétiqueCellular and Molecular Microbiology, Faculté des Sciences, Université libre de Bruxelles (ULB), Boulevard du TriompheSOLEIL Synchrotron, Saint-Aubin - BP48Cellular and Molecular Microbiology, Faculté des Sciences, Université libre de Bruxelles (ULB), Boulevard du TriompheInstitut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien, Département Génomes et GénétiqueCellular and Molecular Microbiology, Faculté des Sciences, Université libre de Bruxelles (ULB), Boulevard du TriompheInstitut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien, Département Génomes et GénétiqueInstitut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien, Département Génomes et GénétiqueAbstract The replication of the two chromosomes in the pathogenic bacterium Vibrio cholerae is coordinated by the binding of initiator protein RctB to a checkpoint sequence, crtS. Replication of crtS on the primary chromosome (Chr1) triggers replication of the secondary chromosome (Chr2), but the details are poorly understood. Here, we analyze RctB binding patterns in the V. cholerae genome across various cell cycle stages. We find that RctB primarily binds to sites inhibiting replication initiation at the Chr2 origin (ori2). This inhibitory effect is counteracted when crtS is replicated on Chr1, causing a shift in RctB binding to sites that activate replication at ori2. Structural analyzes indicate the formation of diverse oligomeric states of RctB, coupled to the allosteric effect of DNA, which determine ori2 accessibility. We propose a synchronization model where, upon replication, crtS locally destabilizes the RctB inhibition complex, releasing the Chr2 replication origin.https://doi.org/10.1038/s41467-024-55598-9 |
| spellingShingle | Théophile Niault Ariel Talavera Eric Le Cam Sonia Baconnais Ole Skovgaard Florian Fournes Léa Wagner Hedvig Tamman Andrew Thompson Dannele Echemendia-Blanco Noa Guzzi Abel Garcia-Pino Didier Mazel Marie-Eve Val Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae Nature Communications |
| title | Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae |
| title_full | Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae |
| title_fullStr | Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae |
| title_full_unstemmed | Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae |
| title_short | Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae |
| title_sort | dynamic transitions of initiator binding coordinate the replication of the two chromosomes in vibrio cholerae |
| url | https://doi.org/10.1038/s41467-024-55598-9 |
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