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Research Article | Molecular Biology and Physiology

RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria

Xiaolong Shao, Weitong Zhang, Mubarak Ishaq Umar, Hei Yuen Wong, Zijing Seng, Yingpeng Xie, Yingchao Zhang, Liang Yang, Chun Kit Kwok, Xin Deng
Yung-Fu Chang, Editor
Xiaolong Shao
aDepartment of Biomedical Sciences, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
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Weitong Zhang
aDepartment of Biomedical Sciences, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
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Mubarak Ishaq Umar
bDepartment of Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
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Hei Yuen Wong
bDepartment of Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
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Zijing Seng
cSingapore Centre for Environmental Life Sciences Engineering (SCELSE), Nanyang Technological University, Singapore
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Yingpeng Xie
aDepartment of Biomedical Sciences, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
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Yingchao Zhang
aDepartment of Biomedical Sciences, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
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Liang Yang
dSchool of Medicine, Southern University of Science and Technology (SUSTech), Shenzhen, Guangdong, China
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  • ORCID record for Liang Yang
Chun Kit Kwok
bDepartment of Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
eShenzhen Research Institute of City University of Hong Kong, Shenzhen, People’s Republic of China
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Xin Deng
aDepartment of Biomedical Sciences, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China
eShenzhen Research Institute of City University of Hong Kong, Shenzhen, People’s Republic of China
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Yung-Fu Chang
College of Veterinary Medicine, Cornell University
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DOI: 10.1128/mBio.02926-19
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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.

  • Copyright © 2020 Shao et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
Xiaolong Shao, Weitong Zhang, Mubarak Ishaq Umar, Hei Yuen Wong, Zijing Seng, Yingpeng Xie, Yingchao Zhang, Liang Yang, Chun Kit Kwok, Xin Deng
mBio Jan 2020, 11 (1) e02926-19; DOI: 10.1128/mBio.02926-19

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RNA G-Quadruplex Structures Mediate Gene Regulation in Bacteria
Xiaolong Shao, Weitong Zhang, Mubarak Ishaq Umar, Hei Yuen Wong, Zijing Seng, Yingpeng Xie, Yingchao Zhang, Liang Yang, Chun Kit Kwok, Xin Deng
mBio Jan 2020, 11 (1) e02926-19; DOI: 10.1128/mBio.02926-19
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KEYWORDS

RNA G-quadruplexes (rG4)
bacteria
gene regulation
nucleic acid structures
prokaryotes
transcriptome-wide

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