The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.

YbeY, a highly conserved protein, is an RNase in E. coli and plays key roles in both processing of the critical 3' end of 16 S rRNA and in 70 S ribosome quality control under stress. These central roles account for YbeY's inclusion in the postulated minimal bacterial genome. However, YbeY...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Maarten Vercruysse, Caroline Köhrer, Bryan W Davies, Markus F F Arnold, John J Mekalanos, Uttam L RajBhandary, Graham C Walker
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2014
Materias:
Acceso en línea:https://doaj.org/article/8e4590c6719e487eb48619c2b1082155
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:8e4590c6719e487eb48619c2b1082155
record_format dspace
spelling oai:doaj.org-article:8e4590c6719e487eb48619c2b10821552021-11-11T06:06:12ZThe highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.1553-73661553-737410.1371/journal.ppat.1004175https://doaj.org/article/8e4590c6719e487eb48619c2b10821552014-06-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24901994/pdf/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374YbeY, a highly conserved protein, is an RNase in E. coli and plays key roles in both processing of the critical 3' end of 16 S rRNA and in 70 S ribosome quality control under stress. These central roles account for YbeY's inclusion in the postulated minimal bacterial genome. However, YbeY is not essential in E. coli although loss of ybeY severely sensitizes it to multiple physiological stresses. Here, we show that YbeY is an essential endoribonuclease in Vibrio cholerae and is crucial for virulence, stress regulation, RNA processing and ribosome quality control, and is part of a core set of RNases essential in most representative pathogens. To understand its function, we analyzed the rRNA and ribosome profiles of a V. cholerae strain partially depleted for YbeY and other RNase mutants associated with 16 S rRNA processing; our results demonstrate that YbeY is also crucial for 16 S rRNA 3' end maturation in V. cholerae and that its depletion impedes subunit assembly into 70 S ribosomes. YbeY's importance to V. cholerae pathogenesis was demonstrated by the complete loss of mice colonization and biofilm formation, reduced cholera toxin production, and altered expression levels of virulence-associated small RNAs of a V. cholerae strain partially depleted for YbeY. Notably, the ybeY genes of several distantly related pathogens can fully complement an E. coli ΔybeY strain under various stress conditions, demonstrating the high conservation of YbeY's activity in stress regulation. Taken together, this work provides the first comprehensive exploration of YbeY's physiological role in a human pathogen, showing its conserved function across species in essential cellular processes.Maarten VercruysseCaroline KöhrerBryan W DaviesMarkus F F ArnoldJohn J MekalanosUttam L RajBhandaryGraham C WalkerPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 10, Iss 6, p e1004175 (2014)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Maarten Vercruysse
Caroline Köhrer
Bryan W Davies
Markus F F Arnold
John J Mekalanos
Uttam L RajBhandary
Graham C Walker
The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.
description YbeY, a highly conserved protein, is an RNase in E. coli and plays key roles in both processing of the critical 3' end of 16 S rRNA and in 70 S ribosome quality control under stress. These central roles account for YbeY's inclusion in the postulated minimal bacterial genome. However, YbeY is not essential in E. coli although loss of ybeY severely sensitizes it to multiple physiological stresses. Here, we show that YbeY is an essential endoribonuclease in Vibrio cholerae and is crucial for virulence, stress regulation, RNA processing and ribosome quality control, and is part of a core set of RNases essential in most representative pathogens. To understand its function, we analyzed the rRNA and ribosome profiles of a V. cholerae strain partially depleted for YbeY and other RNase mutants associated with 16 S rRNA processing; our results demonstrate that YbeY is also crucial for 16 S rRNA 3' end maturation in V. cholerae and that its depletion impedes subunit assembly into 70 S ribosomes. YbeY's importance to V. cholerae pathogenesis was demonstrated by the complete loss of mice colonization and biofilm formation, reduced cholera toxin production, and altered expression levels of virulence-associated small RNAs of a V. cholerae strain partially depleted for YbeY. Notably, the ybeY genes of several distantly related pathogens can fully complement an E. coli ΔybeY strain under various stress conditions, demonstrating the high conservation of YbeY's activity in stress regulation. Taken together, this work provides the first comprehensive exploration of YbeY's physiological role in a human pathogen, showing its conserved function across species in essential cellular processes.
format article
author Maarten Vercruysse
Caroline Köhrer
Bryan W Davies
Markus F F Arnold
John J Mekalanos
Uttam L RajBhandary
Graham C Walker
author_facet Maarten Vercruysse
Caroline Köhrer
Bryan W Davies
Markus F F Arnold
John J Mekalanos
Uttam L RajBhandary
Graham C Walker
author_sort Maarten Vercruysse
title The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.
title_short The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.
title_full The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.
title_fullStr The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.
title_full_unstemmed The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing.
title_sort highly conserved bacterial rnase ybey is essential in vibrio cholerae, playing a critical role in virulence, stress regulation, and rna processing.
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/8e4590c6719e487eb48619c2b1082155
work_keys_str_mv AT maartenvercruysse thehighlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT carolinekohrer thehighlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT bryanwdavies thehighlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT markusffarnold thehighlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT johnjmekalanos thehighlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT uttamlrajbhandary thehighlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT grahamcwalker thehighlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT maartenvercruysse highlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT carolinekohrer highlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT bryanwdavies highlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT markusffarnold highlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT johnjmekalanos highlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT uttamlrajbhandary highlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
AT grahamcwalker highlyconservedbacterialrnaseybeyisessentialinvibriocholeraeplayingacriticalroleinvirulencestressregulationandrnaprocessing
_version_ 1718439512720277504