RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria

ABSTRACT Guanine (G)-rich sequences in RNA can fold into diverse RNA G-quadruplex (rG4) structures to mediate various biological functions and cellular processes in eukaryotic organisms. However, the presence, locations, and functions of rG4s in prokaryotes are still elusive. We used QUMA-1, an rG4-...

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Autores principales:	Xiaolong Shao, Weitong Zhang, Mubarak Ishaq Umar, Hei Yuen Wong, Zijing Seng, Yingpeng Xie, Yingchao Zhang, Liang Yang, Chun Kit Kwok, Xin Deng
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	RNA G-quadruplexes (rG4) bacteria gene regulation nucleic acid structures prokaryotes transcriptome-wide Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ab2a9d7b05db4c51b18363770ff43b89
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spelling	oai:doaj.org-article:ab2a9d7b05db4c51b18363770ff43b892021-11-15T15:56:58ZRNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria10.1128/mBio.02926-192150-7511https://doaj.org/article/ab2a9d7b05db4c51b18363770ff43b892020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02926-19https://doaj.org/toc/2150-7511ABSTRACT Guanine (G)-rich sequences in RNA can fold into diverse RNA G-quadruplex (rG4) structures to mediate various biological functions and cellular processes in eukaryotic organisms. However, the presence, locations, and functions of rG4s in prokaryotes are still elusive. We used QUMA-1, an rG4-specific fluorescent probe, to detect rG4 structures in a wide range of bacterial species both in vitro and in live cells and found rG4 to be an abundant RNA secondary structure across those species. Subsequently, to identify bacterial rG4 sites in the transcriptome, the model Escherichia coli strain and a major human pathogen, Pseudomonas aeruginosa, were subjected to recently developed high-throughput rG4 structure sequencing (rG4-seq). In total, 168 and 161 in vitro rG4 sites were found in E. coli and P. aeruginosa, respectively. Genes carrying these rG4 sites were found to be involved in virulence, gene regulation, cell envelope synthesis, and metabolism. More importantly, biophysical assays revealed the formation of a group of rG4 sites in mRNAs (such as hemL and bswR), and they were functionally validated in cells by genetic (point mutation and lux reporter assays) and phenotypic experiments, providing substantial evidence for the formation and function of rG4s in bacteria. Overall, our study uncovers important regulatory functions of rG4s in bacterial pathogenicity and metabolic pathways and strongly suggests that rG4s exist and can be detected in a wide range of bacterial species. IMPORTANCE G-quadruplex in RNA (rG4) mediates various biological functions and cellular processes in eukaryotic organisms. However, the presence, locations, and functions of rG4 are still elusive in prokaryotes. Here, we found that rG4 is an abundant RNA secondary structure across a wide range of bacterial species. Subsequently, the transcriptome-wide rG4 structure sequencing (rG4-seq) revealed that the model E. coli strain and a major human pathogen, P. aeruginosa, have 168 and 161 in vitro rG4 sites, respectively, involved in virulence, gene regulation, cell envelope, and metabolism. We further verified the regulatory functions of two rG4 sites in bacteria (hemL and bswR). Overall, this finding strongly suggests that rG4s play key regulatory roles in a wide range of bacterial species.Xiaolong ShaoWeitong ZhangMubarak Ishaq UmarHei Yuen WongZijing SengYingpeng XieYingchao ZhangLiang YangChun Kit KwokXin DengAmerican Society for MicrobiologyarticleRNA G-quadruplexes (rG4)bacteriagene regulationnucleic acid structuresprokaryotestranscriptome-wideMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	RNA G-quadruplexes (rG4) bacteria gene regulation nucleic acid structures prokaryotes transcriptome-wide Microbiology QR1-502
spellingShingle	RNA G-quadruplexes (rG4) bacteria gene regulation nucleic acid structures prokaryotes transcriptome-wide Microbiology QR1-502 Xiaolong Shao Weitong Zhang Mubarak Ishaq Umar Hei Yuen Wong Zijing Seng Yingpeng Xie Yingchao Zhang Liang Yang Chun Kit Kwok Xin Deng RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
description	ABSTRACT Guanine (G)-rich sequences in RNA can fold into diverse RNA G-quadruplex (rG4) structures to mediate various biological functions and cellular processes in eukaryotic organisms. However, the presence, locations, and functions of rG4s in prokaryotes are still elusive. We used QUMA-1, an rG4-specific fluorescent probe, to detect rG4 structures in a wide range of bacterial species both in vitro and in live cells and found rG4 to be an abundant RNA secondary structure across those species. Subsequently, to identify bacterial rG4 sites in the transcriptome, the model Escherichia coli strain and a major human pathogen, Pseudomonas aeruginosa, were subjected to recently developed high-throughput rG4 structure sequencing (rG4-seq). In total, 168 and 161 in vitro rG4 sites were found in E. coli and P. aeruginosa, respectively. Genes carrying these rG4 sites were found to be involved in virulence, gene regulation, cell envelope synthesis, and metabolism. More importantly, biophysical assays revealed the formation of a group of rG4 sites in mRNAs (such as hemL and bswR), and they were functionally validated in cells by genetic (point mutation and lux reporter assays) and phenotypic experiments, providing substantial evidence for the formation and function of rG4s in bacteria. Overall, our study uncovers important regulatory functions of rG4s in bacterial pathogenicity and metabolic pathways and strongly suggests that rG4s exist and can be detected in a wide range of bacterial species. IMPORTANCE G-quadruplex in RNA (rG4) mediates various biological functions and cellular processes in eukaryotic organisms. However, the presence, locations, and functions of rG4 are still elusive in prokaryotes. Here, we found that rG4 is an abundant RNA secondary structure across a wide range of bacterial species. Subsequently, the transcriptome-wide rG4 structure sequencing (rG4-seq) revealed that the model E. coli strain and a major human pathogen, P. aeruginosa, have 168 and 161 in vitro rG4 sites, respectively, involved in virulence, gene regulation, cell envelope, and metabolism. We further verified the regulatory functions of two rG4 sites in bacteria (hemL and bswR). Overall, this finding strongly suggests that rG4s play key regulatory roles in a wide range of bacterial species.
format	article
author	Xiaolong Shao Weitong Zhang Mubarak Ishaq Umar Hei Yuen Wong Zijing Seng Yingpeng Xie Yingchao Zhang Liang Yang Chun Kit Kwok Xin Deng
author_facet	Xiaolong Shao Weitong Zhang Mubarak Ishaq Umar Hei Yuen Wong Zijing Seng Yingpeng Xie Yingchao Zhang Liang Yang Chun Kit Kwok Xin Deng
author_sort	Xiaolong Shao
title	RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
title_short	RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
title_full	RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
title_fullStr	RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
title_full_unstemmed	RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
title_sort	rna g-quadruplex structures mediate gene regulation in bacteria
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/ab2a9d7b05db4c51b18363770ff43b89
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RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria

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