Cell cycle constraints on capsulation and bacteriophage susceptibility
Despite the crucial role of bacterial capsules in pathogenesis, it is still unknown if systemic cues such as the cell cycle can control capsule biogenesis. In this study, we show that the capsule of the synchronizable model bacterium Caulobacter crescentus is cell cycle regulated and we unearth a ba...
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doaj-8695eb1caa63442fad07f6a67ff63ce42021-05-04T23:32:42ZengeLife Sciences Publications LtdeLife2050-084X2014-11-01310.7554/eLife.03587Cell cycle constraints on capsulation and bacteriophage susceptibilitySilvia Ardissone0Coralie Fumeaux1Matthieu Bergé2Audrey Beaussart3Laurence Théraulaz4Sunish Kumar Radhakrishnan5Yves F Dufrêne6Patrick H Viollier7Department of Microbiology and Molecular Medicine, Institute of Genetics and Genomics in Geneva, University of Geneva, Geneva, SwitzerlandDepartment of Microbiology and Molecular Medicine, Institute of Genetics and Genomics in Geneva, University of Geneva, Geneva, SwitzerlandDepartment of Microbiology and Molecular Medicine, Institute of Genetics and Genomics in Geneva, University of Geneva, Geneva, SwitzerlandInstitute of Life Sciences, Université catholique de Louvain, Louvain-la-Neuve, BelgiumDepartment of Microbiology and Molecular Medicine, Institute of Genetics and Genomics in Geneva, University of Geneva, Geneva, SwitzerlandDepartment of Microbiology and Molecular Medicine, Institute of Genetics and Genomics in Geneva, University of Geneva, Geneva, SwitzerlandInstitute of Life Sciences, Université catholique de Louvain, Louvain-la-Neuve, BelgiumDepartment of Microbiology and Molecular Medicine, Institute of Genetics and Genomics in Geneva, University of Geneva, Geneva, SwitzerlandDespite the crucial role of bacterial capsules in pathogenesis, it is still unknown if systemic cues such as the cell cycle can control capsule biogenesis. In this study, we show that the capsule of the synchronizable model bacterium Caulobacter crescentus is cell cycle regulated and we unearth a bacterial transglutaminase homolog, HvyA, as restriction factor that prevents capsulation in G1-phase cells. This capsule protects cells from infection by a generalized transducing Caulobacter phage (φCr30), and the loss of HvyA confers insensitivity towards φCr30. Control of capsulation during the cell cycle could serve as a simple means to prevent steric hindrance of flagellar motility or to ensure that phage-mediated genetic exchange happens before the onset of DNA replication. Moreover, the multi-layered regulatory circuitry directing HvyA expression to G1-phase is conserved during evolution, and HvyA orthologues from related Sinorhizobia can prevent capsulation in Caulobacter, indicating that alpha-proteobacteria have retained HvyA activity.https://elifesciences.org/articles/03587capsulecell cycleBTLCPbacteriophagegeneralized transductionCaulobacter crescentus |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Silvia Ardissone Coralie Fumeaux Matthieu Bergé Audrey Beaussart Laurence Théraulaz Sunish Kumar Radhakrishnan Yves F Dufrêne Patrick H Viollier |
spellingShingle |
Silvia Ardissone Coralie Fumeaux Matthieu Bergé Audrey Beaussart Laurence Théraulaz Sunish Kumar Radhakrishnan Yves F Dufrêne Patrick H Viollier Cell cycle constraints on capsulation and bacteriophage susceptibility eLife capsule cell cycle BTLCP bacteriophage generalized transduction Caulobacter crescentus |
author_facet |
Silvia Ardissone Coralie Fumeaux Matthieu Bergé Audrey Beaussart Laurence Théraulaz Sunish Kumar Radhakrishnan Yves F Dufrêne Patrick H Viollier |
author_sort |
Silvia Ardissone |
title |
Cell cycle constraints on capsulation and bacteriophage susceptibility |
title_short |
Cell cycle constraints on capsulation and bacteriophage susceptibility |
title_full |
Cell cycle constraints on capsulation and bacteriophage susceptibility |
title_fullStr |
Cell cycle constraints on capsulation and bacteriophage susceptibility |
title_full_unstemmed |
Cell cycle constraints on capsulation and bacteriophage susceptibility |
title_sort |
cell cycle constraints on capsulation and bacteriophage susceptibility |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2014-11-01 |
description |
Despite the crucial role of bacterial capsules in pathogenesis, it is still unknown if systemic cues such as the cell cycle can control capsule biogenesis. In this study, we show that the capsule of the synchronizable model bacterium Caulobacter crescentus is cell cycle regulated and we unearth a bacterial transglutaminase homolog, HvyA, as restriction factor that prevents capsulation in G1-phase cells. This capsule protects cells from infection by a generalized transducing Caulobacter phage (φCr30), and the loss of HvyA confers insensitivity towards φCr30. Control of capsulation during the cell cycle could serve as a simple means to prevent steric hindrance of flagellar motility or to ensure that phage-mediated genetic exchange happens before the onset of DNA replication. Moreover, the multi-layered regulatory circuitry directing HvyA expression to G1-phase is conserved during evolution, and HvyA orthologues from related Sinorhizobia can prevent capsulation in Caulobacter, indicating that alpha-proteobacteria have retained HvyA activity. |
topic |
capsule cell cycle BTLCP bacteriophage generalized transduction Caulobacter crescentus |
url |
https://elifesciences.org/articles/03587 |
work_keys_str_mv |
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1721476993640300544 |