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.

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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

[Protocol] 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; J. Microbiol. 2022;60(7):659-667. Published online June 22, 2022; DOI: https://doi.org/10.1007/s12275-022-2235-4

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Abstract

Aptamers are short single-stranded DNA or RNA oligonucleotides capable of binding with high affinity and specificity to target molecules. Because of their durability and ease of synthesis, aptamers are used in a wide range of biomedical fields, including the diagnosis of diseases and targeted delivery of therapeutic agents. The aptamers were selected using a process called systematic evolution of ligands by exponential enrichment (SELEX), which has been improved for various research purposes since its development in 1990. In this protocol, we describe a modified SELEX method that rapidly produces high aptamer screening yields using two types of magnetic beads. Using this method, we isolated an aptamer that specifically binds to an antimicrobial peptide. We suggest that by conjugating a small therapeutic-specific aptamer to a gold nanoparticle-based delivery system, which enhances the stability and intracellular delivery of peptides, aptamers selected by our method can be used for the development of therapeutic agents utilizing small therapeutic peptides.

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Recent approaches in the application of antimicrobial peptides in food preservation
Satparkash Singh, Bhavna Jha, Pratiksha Tiwari, Vinay G. Joshi, Adarsh Mishra, Yashpal Singh Malik
World Journal of Microbiology and Biotechnology.2024;[Epub] CrossRef
Design and application of microfluidics in aptamer SELEX and Aptasensors
Shikun Zhang, Yingming Zhang, Zhiyuan Ning, Mengxia Duan, Xianfeng Lin, Nuo Duan, Zhouping Wang, Shijia Wu
Biotechnology Advances.2024; 77: 108461. CrossRef
Nanogenosensors based on aptamers and peptides for bioelectrochemical cancer detection: an overview of recent advances in emerging materials and technologies
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Recent progress of SELEX methods for screening nucleic acid aptamers
Chao Zhu, Ziru Feng, Hongwei Qin, Lu Chen, Mengmeng Yan, Linsen Li, Feng Qu
Talanta.2024; 266: 124998. CrossRef
Aptamer-conjugated gold nanoparticles platform as the intracellular delivery of antibodies for cancer therapy
Ji-Hyun Yeom, Eunkyoung Shin, Hanyong Jin, Haifeng Liu, Yongyang Luo, Youngwoo Nam, Minkyung Ryu, Wooseok Song, Heeyoun Chi, Jeongkyu Kim, Kangseok Lee, Jeehyeon Bae
Journal of Industrial and Engineering Chemistry.2023; 126: 480. CrossRef
Regulation of transforming growth factor-β signaling as a therapeutic approach to treating colorectal cancer
Jana Maslankova, Ivana Vecurkovska, Miroslava Rabajdova, Jana Katuchova, Milos Kicka, Michala Gayova, Vladimir Katuch
World Journal of Gastroenterology.2022; 28(33): 4744. 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.

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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
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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
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Gary Q. Yang, Weibin Cai, Zhiwen Zhang, Yujun Wang
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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
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Yong Chiang Tan, Chandrajit Lahiri
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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

Reviews

Trans-acting regulators of ribonuclease activity: Jaejin Lee , Minho Lee , Kangseok Lee; J. Microbiol. 2021;59(4):341-359. Published online March 29, 2021; DOI: https://doi.org/10.1007/s12275-021-0650-6

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Abstract

RNA metabolism needs to be tightly regulated in response to changes in cellular physiology. Ribonucleases (RNases) play an essential role in almost all aspects of RNA metabolism, including processing, degradation, and recycling of RNA molecules. Thus, living systems have evolved to regulate RNase activity at multiple levels, including transcription, post-transcription, post-translation, and cellular localization. In addition, various trans-acting regulators of RNase activity have been discovered in recent years. This review focuses on the physiological roles and underlying mechanisms of trans-acting regulators of RNase activity.

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
Insights into the metabolism, signaling, and physiological effects of 2’,3’-cyclic nucleotide monophosphates in bacteria
Nick J. Marotta, Emily E. Weinert
Critical Reviews in Biochemistry and Molecular Biology.2023; 58(2-6): 118. 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

Rediscovery of antimicrobial peptides as therapeutic agents: Minkyung Ryu , Jaeyeong Park , Ji-Hyun Yeom , Minju Joo , Kangseok Lee; J. Microbiol. 2021;59(2):113-123. Published online February 1, 2021; DOI: https://doi.org/10.1007/s12275-021-0649-z

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Abstract

In recent years, the occurrence of antibiotic-resistant pathogens is increasing rapidly. There is growing concern as the development of antibiotics is slower than the increase in the resistance of pathogenic bacteria. Antimicrobial peptides (AMPs) are promising alternatives to antibiotics. Despite their name, which implies their antimicrobial activity, AMPs have recently been rediscovered as compounds having antifungal, antiviral, anticancer, antioxidant, and insecticidal effects. Moreover, many AMPs are relatively safe from toxic side effects and the generation of resistant microorganisms due to their target specificity and complexity of the mechanisms underlying their action. In this review, we summarize the history, classification, and mechanisms of action of AMPs, and provide descriptions of AMPs undergoing clinical trials. We also discuss the obstacles associated with the development of AMPs as therapeutic agents and recent strategies formulated to circumvent these obstacles.

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Journal Articles

RNase G controls tpiA mRNA abundance in response to oxygen availability in Escherichia coli: Jaejin Lee , Dong-Ho Lee , Che Ok Jeon , Kangseok Lee; J. Microbiol. 2019;57(10):910-917. Published online September 30, 2019; DOI: https://doi.org/10.1007/s12275-019-9354-6

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Abstract

Studies have shown that many enzymes involved in glycolysis are upregulated in Escherichia coli endoribonuclease G (rng) null mutants. However, the molecular mechanisms underlying the RNase G-associated regulation of glycolysis have not been characterized. Here, we show that RNase G cleaves the 5􍿁􀁇untranslated region of triosephosphate isomerase A (tpiA) mRNA, leading to destabilization of the mRNA in E. coli. Nucleotide substitutions within the RNase G cleavage site in the genome resulted in altered tpiA mRNA stability, indicating that RNase G activity influences tpiA mRNA abundance. In addition, we observed that tpiA expression was enhanced, whereas that of RNase G was decreased, in E. coli cells grown anaerobically. Our findings suggest that RNase G negatively regulates tpiA mRNA abundance in response to oxygen availability in E. coli.

Citations

Citations to this article as recorded by

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
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
Journal of Microbiology.2022; 60(12): 1162. 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
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
The effect of two ribonucleases on the production of Shiga toxin and stx-bearing bacteriophages in Enterohaemorrhagic Escherichia coli
Patricia B. Lodato
Scientific Reports.2021;[Epub] CrossRef
Regulator of ribonuclease activity modulates the pathogenicity of Vibrio vulnificus
Jaejin Lee, Eunkyoung Shin, Jaeyeong Park, Minho Lee, Kangseok Lee
Journal of Microbiology.2021; 59(12): 1133. CrossRef
An alternative miRISC targets a cancer‐associated coding sequence mutation in FOXL2
Eunkyoung Shin, Hanyong Jin, Dae‐Shik Suh, Yongyang Luo, Hye‐Jeong Ha, Tae Heon Kim, Yoonsoo Hahn, Seogang Hyun, Kangseok Lee, Jeehyeon Bae
The EMBO Journal.2020;[Epub] 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

Genome analysis of Rubritalea profundi SAORIC-165T, the first deep-sea verrucomicrobial isolate, from the northwestern Pacific Ocean: Jaeho Song , Ilnam Kang , Yochan Joung , Susumu Yoshizawa , Ryo Kaneko , Kenshiro Oshima , Masahira Hattori , Koji Hamasaki , Soochan Kim , Kangseok Lee , Jang-Cheon Cho; J. Microbiol. 2019;57(5):413-422. Published online February 26, 2019; DOI: https://doi.org/10.1007/s12275-019-8712-8

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Abstract

Although culture-independent studies have shown the presence of Verrucomicrobia in the deep sea, verrucomicrobial strains from deep-sea environments have been rarely cultured and characterized. Recently, Rubritalea profundi SAORIC- 165T, a psychrophilic bacterium of the phylum Verrucomicrobia, was isolated from a depth of 2,000 m in the northwestern Pacific Ocean. In this study, the genome sequence of R. profundi SAORIC-165T, the first deep-sea verrucomicrobial isolate, is reported with description of the genome properties and comparison to surface-borne Rubritalea genomes. The draft genome consisted of four contigs with an entire size of 4,167,407 bp and G+C content of 47.5%. The SAORIC-165T genome was predicted to have 3,844 proteincoding genes and 45 non-coding RNA genes. The genome contained a repertoire of metabolic pathways, including the Embden-Meyerhof-Parnas pathway, pentose phosphate pathway, tricarboxylic acid cycle, assimilatory sulfate reduction, and biosynthesis of nicotinate/nicotinamide, pantothenate/ coenzyme A, folate, and lycopene. The comparative genomic analyses with two surface-derived Rubritalea genomes showed that the SAORIC-165T genome was enriched in genes involved in transposition of mobile elements, signal transduction, and carbohydrate metabolism, some of which might be related to bacterial enhancement of ecological fitness in the deep-sea environment. Amplicon sequencing of 16S rRNA genes from the water column revealed that R. profundi-related phylotypes were relatively abundant at 2,000 m and preferred a particle-associated life style in the deep sea. These findings suggest that R. profundi represents a genetically unique and ecologically relevant verrucomicrobial group well adapted to the deep-sea environment.

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Cultivation of deep-sea bacteria from the Northwest Pacific Ocean and characterization of Limnobacter profundi sp. nov., a phenol-degrading bacterium
Mirae Kim, Jaeho Song, Seung Yeol Shin, Kazuhiro Kogure, Ilnam Kang, Jang-Cheon Cho
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Review

REVIEW] Recent paradigm shift in the assembly of bacterial tripartite efflux pumps and the type I secretion system: Inseong Jo , Jin-Sik Kim , Yongbin Xu , Jaekyung Hyun , Kangseok Lee , Nam-Chul Ha; J. Microbiol. 2019;57(3):185-194. Published online February 26, 2019; DOI: https://doi.org/10.1007/s12275-019-8520-1

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Abstract

Tripartite efflux pumps and the type I secretion system of Gram-negative bacteria are large protein complexes that span the entire cell envelope. These complexes expel antibiotics and other toxic substances or transport protein toxins from bacterial cells. Elucidating the binary and ternary complex structures at an atomic resolution are crucial to understanding the assembly and working mechanism. Recent advances in cryoelectron microscopy along with the construction of chimeric proteins drastically shifted the assembly models. In this review, we describe the current assembly models from a historical perspective and emphasize the common assembly mechanism for the assembly of diverse tripartite pumps and type I secretion systems.

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Molecular mechanisms of antibiotic resistance revisited
Elizabeth M. Darby, Eleftheria Trampari, Pauline Siasat, Maria Solsona Gaya, Ilyas Alav, Mark A. Webber, Jessica M. A. Blair
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Permeation of Fosfomycin through the Phosphate-Specific Channels OprP and OprO of Pseudomonas aeruginosa
Vinaya Kumar Golla, Claudio Piselli, Ulrich Kleinekathöfer, Roland Benz
The Journal of Physical Chemistry B.2022; 126(7): 1388. CrossRef
Adaptation of the periplasm to maintain spatial constraints essential for cell envelope processes and cell viability
Eric Mandela, Christopher J Stubenrauch, David Ryoo, Hyea Hwang, Eli J Cohen, Von L Torres, Pankaj Deo, Chaille T Webb, Cheng Huang, Ralf B Schittenhelm, Morgan Beeby, JC Gumbart, Trevor Lithgow, Iain D Hay
eLife.2022;[Epub] CrossRef
Structure, Assembly, and Function of Tripartite Efflux and Type 1 Secretion Systems in Gram-Negative Bacteria
Ilyas Alav, Jessica Kobylka, Miriam S. Kuth, Klaas M. Pos, Martin Picard, Jessica M. A. Blair, Vassiliy N. Bavro
Chemical Reviews.2021; 121(9): 5479. CrossRef
Biotechnological applications of type 1 secretion systems
Zohreh Pourhassan N., Sander H.J. Smits, Jung Hoon Ahn, Lutz Schmitt
Biotechnology Advances.2021; 53: 107864. CrossRef
Protein-Protein Interactions in the Cytoplasmic Membrane of Escherichia coli: Influence of the Overexpression of Diverse Transporter-Encoding Genes on the Activities of PTS Sugar Uptake Systems
Mohammad Aboulwafa, Zhongge Zhang, Milton H. Saier Jr.
Microbial Physiology.2020; 30(1-6): 36. CrossRef
Perspectives towards antibiotic resistance: from molecules to population
Joon-Hee Lee
Journal of Microbiology.2019; 57(3): 181. CrossRef

Journal Articles

Crystal structure of Streptomyces coelicolor RraAS2, an unusual member of the RNase E inhibitor RraA protein family: Nohra Park , Jihune Heo , Saemee Song , Inseong Jo , Kangseok Lee , Nam-Chul Ha; J. Microbiol. 2017;55(5):388-395. Published online April 29, 2017; DOI: https://doi.org/10.1007/s12275-017-7053-8

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Abstract

Bacterial ribonuclease E (RNase E) plays a crucial role in the processing and decay of RNAs. A small protein named RraA negatively regulates the activity of RNase E via protein-protein interaction in various bacteria. Recently, RraAS1 and RraAS2, which are functional homologs of RraA from Escherichia coli, were identified in the Gram-positive species Streptomyces coelicolor. RraAS1 and RraAS2 inhibit RNase ES ribonuclease activity in S. coelicolor. RraAS1 and RraAS2 have a C-termi-nal extension region unlike typical bacterial RraA proteins. In this study, we present the crystal structure of RraAS2, ex-hibiting a hexamer arranged in a dimer of trimers, consistent with size exclusion chromatographic results. Importantly, the C-terminal extension region formed a long α-helix at the junction of the neighboring subunit, which is similar to the trimeric RraA orthologs from Saccharomyces cerevisiae. Trun-cation of the C-terminal extension region resulted in loss of RNase ES inhibition, demonstrating its crucial role. Our find-ings present the first bacterial RraA that has a hexameric assembly with a C-terminal extension α-helical region, which plays an essential role in the regulation of RNase ES activity in S. coelicolor.

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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
An oxidative metabolic pathway of 4-deoxy-L-erythro-5-hexoseulose uronic acid (DEHU) from alginate in an alginate-assimilating bacterium
Ryuji Nishiyama, Takao Ojima, Yuki Ohnishi, Yasuhiro Kumaki, Tomoyasu Aizawa, Akira Inoue
Communications Biology.2021;[Epub] 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
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
Functional implications of hexameric assembly of RraA proteins from Vibrio vulnificus
Saemee Song, Seokho Hong, Jinyang Jang, Ji-Hyun Yeom, Nohra Park, Jaejin Lee, Yeri Lim, Jun-Yeong Jeon, Hyung-Kyoon Choi, Minho Lee, Nam-Chul Ha, Kangseok Lee, Eric Cascales
PLOS ONE.2017; 12(12): e0190064. CrossRef

RraAS1 inhibits the ribonucleolytic activity of RNase ES by interacting with its catalytic domain in Streptomyces coelicolor: Sojin Seo , Daeyoung Kim , Wooseok Song , Jihune Heo , Minju Joo , Yeri Lim , Ji-Hyun Yeom , Kangseok Lee; J. Microbiol. 2017;55(1):37-43. Published online December 30, 2016; DOI: https://doi.org/10.1007/s12275-017-6518-0

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Abstract

RraA is a protein inhibitor of RNase E, which degrades and processes numerous RNAs in Escherichia coli. Streptomyces coelicolor also contains homologs of RNase E and RraA, RNase ES and RraAS1/RraAS2, respectively. Here, we report that, unlike other RraA homologs, RraAS1 directly interacts with the catalytic domain of RNase ES to exert its inhibitory effect. We further show that rraAS1 gene deletion in S. coelicolor
results
in a higher growth rate and increased production of actinorhodin and undecylprodigiosin, compared with the wild-type strain, suggesting that RraAS1-mediated regulation of RNase ES activity contributes to modulating the cellular physiology of S. coelicolor.

Citations

Citations to this article as recorded by

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
Streptomyces RNases – Function and impact on antibiotic synthesis
George H. Jones
Frontiers in Microbiology.2023;[Epub] 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
Regulator of ribonuclease activity modulates the pathogenicity of Vibrio vulnificus
Jaejin Lee, Eunkyoung Shin, Jaeyeong Park, Minho Lee, Kangseok Lee
Journal of Microbiology.2021; 59(12): 1133. 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
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
Functional implications of hexameric assembly of RraA proteins from Vibrio vulnificus
Saemee Song, Seokho Hong, Jinyang Jang, Ji-Hyun Yeom, Nohra Park, Jaejin Lee, Yeri Lim, Jun-Yeong Jeon, Hyung-Kyoon Choi, Minho Lee, Nam-Chul Ha, Kangseok Lee, Eric Cascales
PLOS ONE.2017; 12(12): e0190064. CrossRef
Crystal structure of Streptomyces coelicolor RraAS2, an unusual member of the RNase E inhibitor RraA protein family
Nohra Park, Jihune Heo, Saemee Song, Inseong Jo, Kangseok Lee, Nam-Chul Ha
Journal of Microbiology.2017; 55(5): 388. CrossRef

RraAS2 requires both scaffold domains of RNase ES for high-affinity binding and inhibitory action on the ribonucleolytic activity: Jihune Heo , Daeyoung Kim , Minju Joo , Boeun Lee , Sojin Seo , Jaejin Lee , Saemee Song , Ji-Hyun Yeom , Nam-Chul Ha , Kangseok Lee; J. Microbiol. 2016;54(10):660-666. Published online September 30, 2016; DOI: https://doi.org/10.1007/s12275-016-6417-9

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Abstract

RraA is a protein inhibitor of RNase E (Rne), which catalyzes the endoribonucleolytic cleavage of a large proportion of RNAs in Escherichia coli. The antibiotic‐producing bacterium Streptomyces coelicolor also contains homologs of RNase E and RraA, designated as RNase ES (Rns), RraAS1, and RraAS2, respectively. Here, we report that RraAS2 requires both scaffold domains of RNase ES for high-affinity binding and inhibitory action on the ribonucleolytic activity. Analyses of the steady-state level of RNase E substrates indicated that coexpression of RraAS2 in E. coli cells overproducing Rns effectively inhibits the ribonucleolytic activity of full-length RNase ES, but its inhibitory effects were moderate or undetectable on other truncated forms of Rns, in which the N- or/and C-terminal scaffold domain was deleted. In addition, RraAS2 more efficiently inhibited the in vitro ribonucleolytic activity of RNase ES than that of a truncated form containing the catalytic domain only. Coimmunoprecipitation and in vivo cross-linking experiments further showed necessity of both scaffold domains of RNase ES for high-affinity binding of RraAS2 to the enzyme, resulting in decreased RNA-binding capacity of RNase ES. Our results indicate that RraAS2 is a protein inhibitor of RNase ES and provide clues to how this inhibitor affects the ribonucleolytic activity of RNase ES.

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Citations to this article as recorded by

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
Streptomyces RNases – Function and impact on antibiotic synthesis
George H. Jones
Frontiers in Microbiology.2023;[Epub] 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
Regulator of ribonuclease activity modulates the pathogenicity of Vibrio vulnificus
Jaejin Lee, Eunkyoung Shin, Jaeyeong Park, Minho Lee, Kangseok Lee
Journal of Microbiology.2021; 59(12): 1133. CrossRef
Divergent rRNAs as regulators of gene expression at the ribosome level
Wooseok Song, Minju Joo, Ji-Hyun Yeom, Eunkyoung Shin, Minho Lee, Hyung-Kyoon Choi, Jihwan Hwang, Yong-In Kim, Ramin Seo, J. Eugene Lee, Christopher J. Moore, Yong-Hak Kim, Seong-il Eyun, Yoonsoo Hahn, Jeehyeon Bae, Kangseok Lee
Nature Microbiology.2019; 4(3): 515. CrossRef
RraAS1 inhibits the ribonucleolytic activity of RNase ES by interacting with its catalytic domain in Streptomyces coelicolor
Sojin Seo, Daeyoung Kim, Wooseok Song, Jihune Heo, Minju Joo, Yeri Lim, Ji-Hyun Yeom, Kangseok Lee
Journal of Microbiology.2017; 55(1): 37. CrossRef
Bdm-Mediated Regulation of Flagellar Biogenesis in Escherichia coli and Salmonella enterica Serovar Typhimurium
Jaejin Lee, Dae-Jun Kim, Ji-Hyun Yeom, Kangseok Lee
Current Microbiology.2017; 74(9): 1015. CrossRef
Functional implications of hexameric assembly of RraA proteins from Vibrio vulnificus
Saemee Song, Seokho Hong, Jinyang Jang, Ji-Hyun Yeom, Nohra Park, Jaejin Lee, Yeri Lim, Jun-Yeong Jeon, Hyung-Kyoon Choi, Minho Lee, Nam-Chul Ha, Kangseok Lee, Eric Cascales
PLOS ONE.2017; 12(12): e0190064. CrossRef
Crystal structure of Streptomyces coelicolor RraAS2, an unusual member of the RNase E inhibitor RraA protein family
Nohra Park, Jihune Heo, Saemee Song, Inseong Jo, Kangseok Lee, Nam-Chul Ha
Journal of Microbiology.2017; 55(5): 388. 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.

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Endoribonuclease-mediated control of hns mRNA stability constitutes a key regulatory pathway for Salmonella Typhimurium pathogenicity island 1 expression
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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
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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
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