Journal of Microbiology

Review

Small regulatory RNAs as key modulators of antibiotic resistance in pathogenic bacteria: Yubin Yang, Hana Hyeon, Minju Joo, Kangseok Lee, Eunkyoung Shin; J. Microbiol. 2025;63(4):e2501027. Published online April 2, 2025; DOI: https://doi.org/10.71150/jm.2501027

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Abstract PDF: The escalating antibiotic resistance crisis poses a significant challenge to global public health, threatening the efficacy of current treatments and driving the emergence of multidrug-resistant pathogens. Among the various factors associated with bacterial antibiotic resistance, small regulatory RNAs (sRNAs) have emerged as pivotal post-transcriptional regulators which orchestrate bacterial adaptation to antibiotic pressure via diverse mechanisms. This review consolidates the current knowledge on sRNA-mediated mechanisms, focusing on drug uptake, drug efflux systems, lipopolysaccharides, cell wall modification, biofilm formation, and mutagenesis. Recent advances in transcriptomics and functional analyses have revealed novel sRNAs and their regulatory networks, expanding our understanding of resistance mechanisms. These findings highlight the potential of targeting sRNA-mediated pathways as an innovative therapeutic strategy to combat antibiotic resistance, and offer promising avenues for managing challenging bacterial infections.

Journal Articles

Relaxed Cleavage Specificity of Hyperactive Variants of Escherichia coli RNase E on RNA I: Dayeong Bae , Hana Hyeon , Eunkyoung Shin , Ji&# , Kangseok Lee; J. Microbiol. 2023;61(2):211-220. Published online February 22, 2023; DOI: https://doi.org/10.1007/s12275-023-00013-z

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RNase E is an essential enzyme in Escherichia coli. The cleavage site of this single-stranded specific endoribonuclease is well-characterized in many RNA substrates. Here, we report that the upregulation of RNase E cleavage activity by a mutation that affects either RNA binding (Q36R) or enzyme multimerization (E429G) was accompanied by relaxed cleavage specificity. Both mutations led to enhanced RNase E cleavage in RNA I, an antisense RNA of ColE1-type plasmid replication, at a major site and other cryptic sites. Expression of a truncated RNA I with a major RNase E cleavage site deletion at the 5′-end (RNA I- 5) resulted in an approximately twofold increase in the steady-state levels of RNA I- 5 and the copy number of ColE1-type plasmid in E. coli cells expressing wild-type or variant RNase E compared to those expressing RNA I. These
results
indicate that RNA I- 5 does not efficiently function as an antisense RNA despite having a triphosphate group at the 5′-end, which protects the RNA from ribonuclease attack. Our study suggests that increased cleavage rates of RNase E lead to relaxed cleavage specificity on RNA I and the inability of the cleavage product of RNA I as an antisense regulator in vivo does not stem from its instability by having 5′-monophosphorylated end.

Citations

Citations to this article as recorded by

Engineering an Escherichia coli based in vivo mRNA manufacturing platform
Edward Curry, George Muir, Jixin Qu, Zoltán Kis, Martyn Hulley, Adam Brown
Biotechnology and Bioengineering.2024; 121(6): 1912. CrossRef

Transcript-specific selective translation by specialized ribosomes bearing genome-encoded heterogeneous rRNAs in V. vulnificus CMCP6: Younkyung Choi , Minju Joo , Wooseok Song , Minho Lee , Hana Hyeon , Hyun-Lee Kim , Ji-Hyun Yeom , Kangseok Lee , Eunkyoung Shin; J. Microbiol. 2022;60(12):1162-1167. Published online November 24, 2022; DOI: https://doi.org/10.1007/s12275-022-2437-9

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Abstract

Ribosomes composed of genome-encoded heterogeneous rRNAs are implicated in the rapid adaptation of bacterial cells to environmental changes. A previous study showed that ribosomes bearing the most heterogeneous rRNAs expressed from the rrnI operon (I-ribosomes) are implicated in the preferential translation of a subset of mRNAs, including hspA and tpiA, in Vibrio vulnificus CMCP6. In this study, we show that HspA nascent peptides were predominantly bound to I-ribosomes. Specifically, I-ribosomes were enriched more than two-fold in ribosomes that were pulled down by immunoprecipitation of HspA peptides compared with the proportion of I-ribosomes in crude ribosomes and ribosomes pulled down by immunoprecipitation of RNA polymerase subunit ß peptides in the wild-type (WT) and rrnI-completed strains. Other methods that utilized the incorporation of an affinity tag in 23S rRNA or chimeric rRNA tethering 16S and 23S rRNAs, which generated specialized functional ribosomes in Escherichia coli, did not result in functional I-ribosomes in V. vulnificus CMCP6. This study provides direct evidence of the preferential translation of hspA mRNA by I-ribosomes.

Citations

Citations to this article as recorded by

Functional conservation of specialized ribosomes bearing genome-encoded variant rRNAs in Vibrio species
Younkyung Choi, Eunkyoung Shin, Minho Lee, Ji-Hyun Yeom, Kangseok Lee, Bashir Sajo Mienda
PLOS ONE.2023; 18(12): e0289072. CrossRef
Relaxed Cleavage Specificity of Hyperactive Variants of Escherichia coli RNase E on RNA I
Dayeong Bae, Hana Hyeon, Eunkyoung Shin, Ji-Hyun Yeom, Kangseok Lee
Journal of Microbiology.2023; 61(2): 211. CrossRef

Gold nanoparticle-DNA aptamer-assisted delivery of antimicrobial peptide effectively inhibits Acinetobacter baumannii infection in mice: Jaeyeong Park , Eunkyoung Shin , Ji-Hyun Yeom , Younkyung Choi , Minju Joo , Minho Lee , Je Hyeong Kim , Jeehyeon Bae , Kangseok Lee; J. Microbiol. 2022;60(1):128-136. Published online December 29, 2021; DOI: https://doi.org/10.1007/s12275-022-1620-3

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Abstract

Acinetobacter baumannii causes multidrug resistance, leading to fatal infections in humans. In this study, we showed that Lys AB2 P3-His–a hexahistidine-tagged form of an antimicrobial peptide (AMP) loaded onto DNA aptamer-functionalized gold nanoparticles (AuNP-Apt)–can effectively inhibit A. baumannii infection in mice. When A. baumannii-infected mice were intraperitoneally injected with AuNP-Apt loaded with Lys AB2 P3-His, a marked reduction in A. baumannii colonization was observed in the mouse organs, leading to prominently increased survival time and rate of the mice compared to those of the control mice treated with AuNP-Apt or Lys AB2 P3-His only. This study shows that AMPs loaded onto AuNP-Apt could be an effective therapeutic tool against infections caused by multidrug-resistant pathogenic bacteria in humans.

Citations

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Challenges and Emerging Molecular Approaches in Combating Antimicrobial Resistance
Gene Philip Levee Ynion, Christian Jay Rosal, Arvin Zulueta, Angelo Ordanel, Christopher Marlowe Caipang
Journal of Bacteriology and Virology.2024; 54(1): 12. CrossRef
Gold Nanoparticles and Antimicrobial Peptides: A Novel Combination
Şule Balcı, Bengü Ergüden
ChemistrySelect.2024;[Epub] CrossRef
Aptamers: A Cutting-Edge Approach for Gram-Negative Bacterial Pathogen Identification
María Guadalupe Córdova-Espinoza, Rosa González-Vázquez, Rolando Rafik Barron-Fattel, Raquel Gónzalez-Vázquez, Marco Antonio Vargas-Hernández, Exsal Manuel Albores-Méndez, Ana Laura Esquivel-Campos, Felipe Mendoza-Pérez, Lino Mayorga-Reyes, María Angélica
International Journal of Molecular Sciences.2024; 25(2): 1257. CrossRef
Antimicrobial Peptide Delivery Systems as Promising Tools Against Resistant Bacterial Infections
Kamila Botelho Sampaio de Oliveira, Michel Lopes Leite, Nadielle Tamires Moreira Melo, Letícia Ferreira Lima, Talita Cristina Queiroz Barbosa, Nathalia Lira Carmo, Douglas Afonso Bittencourt Melo, Hugo Costa Paes, Octávio Luiz Franco
Antibiotics.2024; 13(11): 1042. CrossRef
Optimizing Treatment for Carbapenem-Resistant Acinetobacter baumannii Complex Infections: A Review of Current Evidence
Seong Jin Choi, Eu Suk Kim
Infection & Chemotherapy.2024; 56(2): 171. CrossRef
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Fatemeh Karimzadeh, Elahe Soltani Fard, Akram Nadi, Rahim Malekzadeh, Fatemeh Elahian, Seyed Abbas Mirzaei
Journal of Materials Chemistry B.2024; 12(25): 6033. CrossRef
Colistin Resistance Mechanism and Management Strategies of Colistin-Resistant Acinetobacter baumannii Infections
Md Minarul Islam, Da Eun Jung, Woo Shik Shin, Man Hwan Oh
Pathogens.2024; 13(12): 1049. CrossRef
Progress in Programmable DNA-Aided Self-Assembly of the Master Frame of a Drug Delivery System
Gary Q. Yang, Weibin Cai, Zhiwen Zhang, Yujun Wang
ACS Applied Bio Materials.2023; 6(12): 5125. CrossRef
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Sara M. Robledo, Silvia Pérez-Silanes, Celia Fernández-Rubio, Ana Poveda, Lianet Monzote, Víctor M. González, Paloma Alonso-Collado, Javier Carrión
Pathogens.2023; 12(7): 939. CrossRef
Applications and Challenges of Bacteriostatic Aptamers in the Treatment of Common Pathogenic Bacteria Infections
Diandian Li, Yuan Su, Jie Li, Rong Liu, Bing Fang, Jingjing He, Wentao Xu, Longjiao Zhu
Biomacromolecules.2023; 24(11): 4568. CrossRef
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Yong Chiang Tan, Chandrajit Lahiri
Frontiers in Immunology.2022;[Epub] CrossRef
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Preeti Garg, Prerna Attri, Rohit Sharma, Moondeep Chauhan, Ganga Ram Chaudhary
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Aptamer Decorated Emodin Nanoparticles-Assisted Delivery of Dermcidin-Derived Peptide DCD-1L: Photoactive Bio-Theragnostic Agent for Enterococcus Faecalis Biofilm Destruction
Maryam Pourhajibagher, Abbas Bahador
SSRN Electronic Journal .2022;[Epub] CrossRef
Development of DNA aptamers specific for small therapeutic peptides using a modified SELEX method
Jaemin Lee, Minkyung Ryu, Dayeong Bae, Hong-Man Kim, Seong-il Eyun, Jeehyeon Bae, Kangseok Lee
Journal of Microbiology.2022; 60(7): 659. CrossRef
Aptamer decorated emodin nanoparticles-assisted delivery of dermcidin-derived peptide DCD-1L: Photoactive bio-theragnostic agent for Enterococcus faecalis biofilm destruction
Maryam Pourhajibagher, Abbas Bahador
Photodiagnosis and Photodynamic Therapy.2022; 39: 103020. CrossRef

Regulator of ribonuclease activity modulates the pathogenicity of Vibrio vulnificus: Jaejin Lee , Eunkyoung Shin , Jaeyeong Park , Minho Lee , Kangseok Lee; J. Microbiol. 2021;59(12):1133-1141. Published online November 9, 2021; DOI: https://doi.org/10.1007/s12275-021-1518-5

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Abstract

RraA, a protein regulator of RNase E activity, plays a unique role in modulating the mRNA abundance in Escherichia coli. The marine pathogenic bacterium Vibrio vulnificus also possesses homologs of RNase E (VvRNase E) and RraA (VvRraA1 and VvRraA2). However, their physiological roles have not yet been investigated. In this study, we demonstrated that VvRraA1 expression levels affect the pathogenicity of V. vulnificus. Compared to the wild-type strain, the VvrraA1-deleted strain (ΔVvrraA1) showed decreased motility, invasiveness, biofilm formation ability as well as virulence in mice; these phenotypic changes of ΔVvrraA1 were restored by the exogenous expression of VvrraA1. Transcriptomic analysis indicated that VvRraA1 expression levels affect the abundance of a large number of mRNA species. Among them, the halflives of mRNA species encoding virulence factors (e.g., smcR and htpG) that have been previously shown to affect VvrraA1 expression-dependent phenotypes were positively correlated with VvrraA1 expression levels. These findings suggest that VvRraA1 modulates the pathogenicity of V. vulnificus by regulating the abundance of a subset of mRNA species.

Citations

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Identification of the global regulatory roles of RraA via the integrative transcriptome and proteome in Vibrio alginolyticus
Huizhen Chen, Qian Gao, Bing Liu, Ying Zhang, Jianxiang Fang, Songbiao Wang, Youqi Chen, Chang Chen, Nicolas E. Buchler
mSphere.2024;[Epub] CrossRef
Comparative Transcriptomic Analysis of Flagellar-Associated Genes in Salmonella Typhimurium and Its rnc Mutant
Seungmok Han, Ji-Won Byun, Minho Lee
Journal of Microbiology.2024; 62(1): 33. CrossRef
Eco-Evolutionary Drivers of Vibrio parahaemolyticus Sequence Type 3 Expansion: Retrospective Machine Learning Approach
Amy Marie Campbell, Chris Hauton, Ronny van Aerle, Jaime Martinez-Urtaza
JMIR Bioinformatics and Biotechnology.2024; 5: e62747. CrossRef
Relaxed Cleavage Specificity of Hyperactive Variants of Escherichia coli RNase E on RNA I
Dayeong Bae, Hana Hyeon, Eunkyoung Shin, Ji-Hyun Yeom, Kangseok Lee
Journal of Microbiology.2023; 61(2): 211. CrossRef
Regulator of RNase E activity modulates the pathogenicity of Salmonella Typhimurium
Jaejin Lee, Eunkyoung Shin, Ji-Hyun Yeom, Jaeyoung Park, Sunwoo Kim, Minho Lee, Kangseok Lee
Microbial Pathogenesis.2022; 165: 105460. CrossRef

Review

MINIREVIEW] Regulation of Escherichia coli RNase III activity: Boram Lim , Minji Sim , Howoon Lee , Seogang Hyun , Younghoon Lee , Yoonsoo Hahn , Eunkyoung Shin , Kangseok Lee; J. Microbiol. 2015;53(8):487-494. Published online July 31, 2015; DOI: https://doi.org/10.1007/s12275-015-5323-x

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Abstract

Bacterial cells respond to changes in the environment by adjusting their physiological reactions. In cascades of cellular responses to stresses of various origins, rapid modulation of RNA function is known to be an effective biochemical adaptation. Among many factors affecting RNA function, RNase III, a member of the phylogenetically highly conserved endoribonuclease III family, plays a key role in posttranscriptional regulatory pathways in Escherichia coli. In this review, we provide an overview of the factors affecting RNase III activity in E. coli.

Citations

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Comparative Transcriptomic Analysis of Flagellar-Associated Genes in Salmonella Typhimurium and Its rnc Mutant
Seungmok Han, Ji-Won Byun, Minho Lee
Journal of Microbiology.2024; 62(1): 33. CrossRef
arfAantisense RNA regulates MscL excretory activity
Rosa Morra, Fenryco Pratama, Thomas Butterfield, Geizecler Tomazetto, Kate Young, Ruth Lopez, Neil Dixon
Life Science Alliance.2023; 6(6): e202301954. CrossRef
Transcriptome and metabolome analyses of response of Synechocystis sp. PCC 6803 to methyl viologen
Xinyu Hu, Tianyuan Zhang, Kai Ji, Ke Luo, Li Wang, Wenli Chen
Applied Microbiology and Biotechnology.2021; 105(21-22): 8377. CrossRef
Endoribonuclease-mediated control of hns mRNA stability constitutes a key regulatory pathway for Salmonella Typhimurium pathogenicity island 1 expression
Minho Lee, Minkyung Ryu, Minju Joo, Young-Jin Seo, Jaejin Lee, Hong-Man Kim, Eunkyoung Shin, Ji-Hyun Yeom, Yong-Hak Kim, Jeehyeon Bae, Kangseok Lee, William Navarre
PLOS Pathogens.2021; 17(2): e1009263. CrossRef
Trans-acting regulators of ribonuclease activity
Jaejin Lee, Minho Lee, Kangseok Lee
Journal of Microbiology.2021; 59(4): 341. CrossRef
RNase III, Ribosome Biogenesis and Beyond
Maxence Lejars, Asaki Kobayashi, Eliane Hajnsdorf
Microorganisms.2021; 9(12): 2608. CrossRef
The rnc Gene Regulates the Microstructure of Exopolysaccharide in the Biofilm of Streptococcus mutans through the β-Monosaccharides
Yangyu Lu, Hongyu Zhang, Meng Li, Mengying Mao, Jiaqi Song, Yalan Deng, Lei Lei, Yingming Yang, Tao Hu
Caries Research.2021; 55(5): 534. CrossRef
Distributive enzyme binding controlled by local RNA context results in 3′ to 5′ directional processing of dicistronic tRNA precursors byEscherichia coliribonuclease P
Jing Zhao, Michael E Harris
Nucleic Acids Research.2019; 47(3): 1451. CrossRef
RNase G controls tpiA mRNA abundance in response to oxygen availability in Escherichia coli
Jaejin Lee, Dong-Ho Lee, Che Ok Jeon, Kangseok Lee
Journal of Microbiology.2019; 57(10): 910. CrossRef
The coordinated action of RNase III and RNase G controls enolase expression in response to oxygen availability in Escherichia coli
Minho Lee, Minju Joo, Minji Sim, Se-Hoon Sim, Hyun-Lee Kim, Jaejin Lee, Minkyung Ryu, Ji-Hyun Yeom, Yoonsoo Hahn, Nam-Chul Ha, Jang-Cheon Cho, Kangseok Lee
Scientific Reports.2019;[Epub] CrossRef
Identification of endoribonuclease specific cleavage positions reveals novel targets of RNase III inStreptococcus pyogenes
Anaïs Le Rhun, Anne-Laure Lécrivain, Johan Reimegård, Estelle Proux-Wéra, Laura Broglia, Cristina Della Beffa, Emmanuelle Charpentier
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Regulation and functions of bacterial PNPase
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