Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>

ABSTRACT Posttranscriptional regulation plays an essential role in the quick adaptation of pathogenic bacteria to host environments, and RNases play key roles in this process by modifying small RNAs and mRNAs. We find that the Pseudomonas aeruginosa endonuclease YbeY is required for rRNA processing...

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Autores principales:	Yushan Xia, Yuding Weng, Congjuan Xu, Dan Wang, Xiaolei Pan, Zhenyang Tian, Bin Xia, Haozhou Li, Ronghao Chen, Chang Liu, Yongxin Jin, Fang Bai, Zhihui Cheng, Oscar P. Kuipers, Weihui Wu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	endoribonuclease Pseudomonas aeruginosa ReaL RpoS YbeY Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a20a993afdc2485cbe06b3e3837ce7c1
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spelling	oai:doaj.org-article:a20a993afdc2485cbe06b3e3837ce7c12021-11-15T15:56:47ZEndoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>10.1128/mBio.00659-202150-7511https://doaj.org/article/a20a993afdc2485cbe06b3e3837ce7c12020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00659-20https://doaj.org/toc/2150-7511ABSTRACT Posttranscriptional regulation plays an essential role in the quick adaptation of pathogenic bacteria to host environments, and RNases play key roles in this process by modifying small RNAs and mRNAs. We find that the Pseudomonas aeruginosa endonuclease YbeY is required for rRNA processing and the bacterial virulence in a murine acute pneumonia model. Transcriptomic analyses reveal that knocking out the ybeY gene results in downregulation of oxidative stress response genes, including the catalase genes katA and katB. Consistently, the ybeY mutant is more susceptible to H2O2 and neutrophil-mediated killing. Overexpression of katA restores the bacterial tolerance to H2O2 and neutrophil killing as well as virulence. We further find that the downregulation of the oxidative stress response genes is due to defective expression of the stationary-phase sigma factor RpoS. We demonstrate an autoregulatory mechanism of RpoS and find that ybeY mutation increases the level of a small RNA, ReaL, which directly represses the translation of rpoS through the 5′ UTR of its mRNA and subsequently reduces the expression of the oxidative stress response genes. In vitro assays demonstrate direct degradation of ReaL by YbeY. Deletion of reaL or overexpression of rpoS in the ybeY mutant restores the bacterial tolerance to oxidative stress and the virulence. We also demonstrate that YbeZ binds to YbeY and is involved in the 16S rRNA processing and regulation of reaL and rpoS as well as the bacterial virulence. Overall, our results reveal pleiotropic roles of YbeY and the YbeY-mediated regulation of rpoS through ReaL. IMPORTANCE The increasing bacterial antibiotic resistance imposes a severe threat to human health. For the development of effective treatment and prevention strategies, it is critical to understand the mechanisms employed by bacteria to grow in the human body. Posttranscriptional regulation plays an important role in bacterial adaptation to environmental changes. RNases and small RNAs are key players in this regulation. In this study, we demonstrate critical roles of the RNase YbeY in the virulence of the pathogenic bacterium Pseudomonas aeruginosa. We further identify the small RNA ReaL as the direct target of YbeY and elucidate the YbeY-regulated pathway on the expression of bacterial virulence factors. Our results shed light on the complex regulatory network of P. aeruginosa and indicate that inference with the YbeY-mediated regulatory pathway might be a valid strategy for the development of a novel treatment strategy.Yushan XiaYuding WengCongjuan XuDan WangXiaolei PanZhenyang TianBin XiaHaozhou LiRonghao ChenChang LiuYongxin JinFang BaiZhihui ChengOscar P. KuipersWeihui WuAmerican Society for MicrobiologyarticleendoribonucleasePseudomonas aeruginosaReaLRpoSYbeYMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	endoribonuclease Pseudomonas aeruginosa ReaL RpoS YbeY Microbiology QR1-502
spellingShingle	endoribonuclease Pseudomonas aeruginosa ReaL RpoS YbeY Microbiology QR1-502 Yushan Xia Yuding Weng Congjuan Xu Dan Wang Xiaolei Pan Zhenyang Tian Bin Xia Haozhou Li Ronghao Chen Chang Liu Yongxin Jin Fang Bai Zhihui Cheng Oscar P. Kuipers Weihui Wu Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
description	ABSTRACT Posttranscriptional regulation plays an essential role in the quick adaptation of pathogenic bacteria to host environments, and RNases play key roles in this process by modifying small RNAs and mRNAs. We find that the Pseudomonas aeruginosa endonuclease YbeY is required for rRNA processing and the bacterial virulence in a murine acute pneumonia model. Transcriptomic analyses reveal that knocking out the ybeY gene results in downregulation of oxidative stress response genes, including the catalase genes katA and katB. Consistently, the ybeY mutant is more susceptible to H2O2 and neutrophil-mediated killing. Overexpression of katA restores the bacterial tolerance to H2O2 and neutrophil killing as well as virulence. We further find that the downregulation of the oxidative stress response genes is due to defective expression of the stationary-phase sigma factor RpoS. We demonstrate an autoregulatory mechanism of RpoS and find that ybeY mutation increases the level of a small RNA, ReaL, which directly represses the translation of rpoS through the 5′ UTR of its mRNA and subsequently reduces the expression of the oxidative stress response genes. In vitro assays demonstrate direct degradation of ReaL by YbeY. Deletion of reaL or overexpression of rpoS in the ybeY mutant restores the bacterial tolerance to oxidative stress and the virulence. We also demonstrate that YbeZ binds to YbeY and is involved in the 16S rRNA processing and regulation of reaL and rpoS as well as the bacterial virulence. Overall, our results reveal pleiotropic roles of YbeY and the YbeY-mediated regulation of rpoS through ReaL. IMPORTANCE The increasing bacterial antibiotic resistance imposes a severe threat to human health. For the development of effective treatment and prevention strategies, it is critical to understand the mechanisms employed by bacteria to grow in the human body. Posttranscriptional regulation plays an important role in bacterial adaptation to environmental changes. RNases and small RNAs are key players in this regulation. In this study, we demonstrate critical roles of the RNase YbeY in the virulence of the pathogenic bacterium Pseudomonas aeruginosa. We further identify the small RNA ReaL as the direct target of YbeY and elucidate the YbeY-regulated pathway on the expression of bacterial virulence factors. Our results shed light on the complex regulatory network of P. aeruginosa and indicate that inference with the YbeY-mediated regulatory pathway might be a valid strategy for the development of a novel treatment strategy.
format	article
author	Yushan Xia Yuding Weng Congjuan Xu Dan Wang Xiaolei Pan Zhenyang Tian Bin Xia Haozhou Li Ronghao Chen Chang Liu Yongxin Jin Fang Bai Zhihui Cheng Oscar P. Kuipers Weihui Wu
author_facet	Yushan Xia Yuding Weng Congjuan Xu Dan Wang Xiaolei Pan Zhenyang Tian Bin Xia Haozhou Li Ronghao Chen Chang Liu Yongxin Jin Fang Bai Zhihui Cheng Oscar P. Kuipers Weihui Wu
author_sort	Yushan Xia
title	Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_short	Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full	Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_fullStr	Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full_unstemmed	Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_sort	endoribonuclease ybey is essential for rna processing and virulence in <named-content content-type="genus-species">pseudomonas aeruginosa</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/a20a993afdc2485cbe06b3e3837ce7c1
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Endoribonuclease YbeY Is Essential for RNA Processing and Virulence in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>

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