A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity

ABSTRACT BolA family proteins are conserved in Gram-negative bacteria and many eukaryotes. While diverse cellular phenotypes have been linked to this protein family, the molecular pathways through which these proteins mediate their effects are not well described. Here, we investigated the roles of B...

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Autores principales:	Aurore Fleurie, Abdelrahim Zoued, Laura Alvarez, Kelly M. Hines, Felipe Cava, Libin Xu, Brigid M. Davis, Matthew K. Waldor
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	BolA IbaG Vibrio cholerae cell envelope cell shape iron-sulfur cluster Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/33ca789961c04e5b83d94e3691620288
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spelling	oai:doaj.org-article:33ca789961c04e5b83d94e36916202882021-11-15T16:22:10ZA <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity10.1128/mBio.00790-192150-7511https://doaj.org/article/33ca789961c04e5b83d94e36916202882019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00790-19https://doaj.org/toc/2150-7511ABSTRACT BolA family proteins are conserved in Gram-negative bacteria and many eukaryotes. While diverse cellular phenotypes have been linked to this protein family, the molecular pathways through which these proteins mediate their effects are not well described. Here, we investigated the roles of BolA family proteins in Vibrio cholerae, the cholera pathogen. Like Escherichia coli, V. cholerae encodes two BolA proteins, BolA and IbaG. However, in marked contrast to E. coli, where bolA is linked to cell shape and ibaG is not, in V. cholerae, bolA mutants lack morphological defects, whereas ibaG proved critical for the generation and/or maintenance of the pathogen’s morphology. Notably, the bizarre-shaped, multipolar, elongated, and wide cells that predominated in exponential-phase ΔibaG V. cholerae cultures were not observed in stationary-phase cultures. The V. cholerae ΔibaG mutant exhibited increased sensitivity to cell envelope stressors, including cell wall-acting antibiotics and bile, and was defective in intestinal colonization. ΔibaG V. cholerae had reduced peptidoglycan and lipid II and altered outer membrane lipids, likely contributing to the mutant’s morphological defects and sensitivity to envelope stressors. Transposon insertion sequencing analysis of ibaG’s genetic interactions suggested that ibaG is involved in several processes involved in the generation and homeostasis of the cell envelope. Furthermore, copurification studies revealed that IbaG interacts with proteins containing iron-sulfur clusters or involved in their assembly. Collectively, our findings suggest that V. cholerae IbaG controls cell morphology and cell envelope integrity through its role in biogenesis or trafficking of iron-sulfur cluster proteins. IMPORTANCE BolA-like proteins are conserved across prokaryotes and eukaryotes. These proteins have been linked to a variety of phenotypes, but the pathways and mechanisms through which they act have not been extensively characterized. Here, we unraveled the role of the BolA-like protein IbaG in the cholera pathogen Vibrio cholerae. The absence of IbaG was associated with dramatic changes in cell morphology, sensitivity to envelope stressors, and intestinal colonization defects. IbaG was found to be required for biogenesis of several components of the V. cholerae cell envelope and to interact with numerous iron-sulfur cluster-containing proteins and factors involved in their assembly. Thus, our findings suggest that IbaG governs V. cholerae cell shape and cell envelope homeostasis through its effects on iron-sulfur proteins and associated pathways. The diversity of processes involving iron-sulfur-containing proteins is likely a factor underlying the range of phenotypes associated with BolA family proteins.Aurore FleurieAbdelrahim ZouedLaura AlvarezKelly M. HinesFelipe CavaLibin XuBrigid M. DavisMatthew K. WaldorAmerican Society for MicrobiologyarticleBolAIbaGVibrio choleraecell envelopecell shapeiron-sulfur clusterMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	BolA IbaG Vibrio cholerae cell envelope cell shape iron-sulfur cluster Microbiology QR1-502
spellingShingle	BolA IbaG Vibrio cholerae cell envelope cell shape iron-sulfur cluster Microbiology QR1-502 Aurore Fleurie Abdelrahim Zoued Laura Alvarez Kelly M. Hines Felipe Cava Libin Xu Brigid M. Davis Matthew K. Waldor A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity
description	ABSTRACT BolA family proteins are conserved in Gram-negative bacteria and many eukaryotes. While diverse cellular phenotypes have been linked to this protein family, the molecular pathways through which these proteins mediate their effects are not well described. Here, we investigated the roles of BolA family proteins in Vibrio cholerae, the cholera pathogen. Like Escherichia coli, V. cholerae encodes two BolA proteins, BolA and IbaG. However, in marked contrast to E. coli, where bolA is linked to cell shape and ibaG is not, in V. cholerae, bolA mutants lack morphological defects, whereas ibaG proved critical for the generation and/or maintenance of the pathogen’s morphology. Notably, the bizarre-shaped, multipolar, elongated, and wide cells that predominated in exponential-phase ΔibaG V. cholerae cultures were not observed in stationary-phase cultures. The V. cholerae ΔibaG mutant exhibited increased sensitivity to cell envelope stressors, including cell wall-acting antibiotics and bile, and was defective in intestinal colonization. ΔibaG V. cholerae had reduced peptidoglycan and lipid II and altered outer membrane lipids, likely contributing to the mutant’s morphological defects and sensitivity to envelope stressors. Transposon insertion sequencing analysis of ibaG’s genetic interactions suggested that ibaG is involved in several processes involved in the generation and homeostasis of the cell envelope. Furthermore, copurification studies revealed that IbaG interacts with proteins containing iron-sulfur clusters or involved in their assembly. Collectively, our findings suggest that V. cholerae IbaG controls cell morphology and cell envelope integrity through its role in biogenesis or trafficking of iron-sulfur cluster proteins. IMPORTANCE BolA-like proteins are conserved across prokaryotes and eukaryotes. These proteins have been linked to a variety of phenotypes, but the pathways and mechanisms through which they act have not been extensively characterized. Here, we unraveled the role of the BolA-like protein IbaG in the cholera pathogen Vibrio cholerae. The absence of IbaG was associated with dramatic changes in cell morphology, sensitivity to envelope stressors, and intestinal colonization defects. IbaG was found to be required for biogenesis of several components of the V. cholerae cell envelope and to interact with numerous iron-sulfur cluster-containing proteins and factors involved in their assembly. Thus, our findings suggest that IbaG governs V. cholerae cell shape and cell envelope homeostasis through its effects on iron-sulfur proteins and associated pathways. The diversity of processes involving iron-sulfur-containing proteins is likely a factor underlying the range of phenotypes associated with BolA family proteins.
format	article
author	Aurore Fleurie Abdelrahim Zoued Laura Alvarez Kelly M. Hines Felipe Cava Libin Xu Brigid M. Davis Matthew K. Waldor
author_facet	Aurore Fleurie Abdelrahim Zoued Laura Alvarez Kelly M. Hines Felipe Cava Libin Xu Brigid M. Davis Matthew K. Waldor
author_sort	Aurore Fleurie
title	A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity
title_short	A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity
title_full	A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity
title_fullStr	A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity
title_full_unstemmed	A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity
title_sort	<named-content content-type="genus-species">vibrio cholerae</named-content> bola-like protein is required for proper cell shape and cell envelope integrity
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/33ca789961c04e5b83d94e3691620288
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A <named-content content-type="genus-species">Vibrio cholerae</named-content> BolA-Like Protein Is Required for Proper Cell Shape and Cell Envelope Integrity

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