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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Main Authors: Silvia Ardissone, Coralie Fumeaux, Matthieu Bergé, Audrey Beaussart, Laurence Théraulaz, Sunish Kumar Radhakrishnan, Yves F Dufrêne, Patrick H Viollier
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2014-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/03587
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spelling 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
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