Journal of Microbiology

Review

Recent trends in dual-acting hybrid antibiotics and combination therapies against Gram-negative pathogens: Ji Eun Son, Umji Choi, Gyubin Han, Jeongho Lee, Chang-Ro Lee; J. Microbiol. 2026;64(3):e2601004. Published online March 31, 2026; DOI: https://doi.org/10.71150/jm.2601004

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Antibiotic resistance poses a serious challenge to public health worldwide; however, the development of new antibiotic classes for combating bacterial infections, especially those caused by Gram-negative pathogens, has slowed in recent years. Dual-acting hybrid antibiotics with a metabolically non-cleavable covalent bond represent an emerging strategy for developing novel antibiotic classes to overcome antibiotic resistance. The covalent connection between two antibiotics results in a fixed pharmacokinetic profile of a single molecule and can impede bacterial efflux. However, as most antibiotics do not have membrane-destabilizing activity, the resulting increase in molecular weight by connection of two antibiotics could limit their activity against Gram-negative bacteria, whose outer membrane forms a strong barrier blocking the penetration of high-molecular weight antibiotics. Here, we review recent developments in dual-acting hybrid antibiotics targeting Gram-negative bacteria, with a focus on their antibacterial efficacy. We also discuss combination therapy strategies in which the underlying molecular mechanisms of synergy have been characterized. Finally, we outline future directions for the rational design of hybrid antibiotics against Gram-negative pathogens.

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Pioneering strategies for overcoming bacterial drug resistance
Byoung Sik Kim
Journal of Microbiology.2026; 64(3): e2603100. CrossRef

Articles

Inhibition of cardiolipin biosynthesis partially suppresses the sensitivity of an Escherichia coli mutant lacking OmpC to envelope stress: Dae-Beom Ryu, Umji Choi, Gyubin Han, Chang-Ro Lee; J. Microbiol. 2025;63(11):e2507004. Published online November 30, 2025; DOI: https://doi.org/10.71150/jm.2507004

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Abstract PDF Supplementary Material: Porins in the outer membrane (OM) of Gram-negative bacteria play two main functions: passage of various extracellular molecules and maintenance of membrane integrity. OmpC, a non-specific porin, is involved in both functions; however, the exact mechanism of maintenance of membrane integrity remains unknown. In this study, we found that inhibiting cardiolipin biosynthesis partially restored the growth defect of the ompC mutant under envelope stress. Among the three enzymes involved in cardiolipin biosynthesis, ClsABC, this effect is primarily associated with ClsA. Notably, the deletion of ClsA also suppressed the similar phenotypes of an Escherichia coli mutant lacking YhdP, a transmembrane protein involved in phospholipid transport from the inner membrane to the OM. Collectively, these results imply that OmpC may contribute to membrane integrity, partially through mechanisms linked to transport or biosynthesis of phospholipids such as cardiolipin.

The inner membrane protein LapB is required for adaptation to cold stress in an LpxC-independent manner: Han Byeol Lee , Si Hyoung Park , Chang-Ro Lee; J. Microbiol. 2021;59(7):666-674. Published online May 15, 2021; DOI: https://doi.org/10.1007/s12275-021-1130-8

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Abstract PDF

The inner membrane protein lipopolysaccharide assembly protein B (LapB) is an adaptor protein that activates the proteolysis of LpxC by an essential inner membrane metalloprotease, FtsH, leading to a decrease in the level of lipopolysaccharide in the membrane. In this study, we revealed the mechanism by which the essential inner membrane protein YejM regulates LapB and analyzed the role of the transmembrane domain of LapB in Escherichia coli. The transmembrane domain of YejM genetically and physically interacted with LapB and inhibited its function, which led to the accumulation of LpxC. The transmembrane domain of LapB was indispensable for both its physical interaction with YejM and its regulation of LpxC proteolysis. Notably, we found that the lapB mutant exhibited strong cold sensitivity and this phenotype was not associated with increased accumulation of LpxC. The transmembrane domain of LapB was also required for its role in adaptation to cold stress. Taken together, these
results
showed that LapB plays an important role in both the regulation of LpxC level, which is controlled by its interaction with the transmembrane domain of YejM, and adaptation to cold stress, which is independent of LpxC.

Citations

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Bile and short-chain fatty acid salts affect survival and virulence of Klebsiella Oxytoca of mussel origin
Jingjing Xu, Meng Sun, Jiangcheng Chang, Qingchao Xie, Yongjie Wang, Lanming Chen
Archives of Microbiology.2025;[Epub] CrossRef
Inhibition of cardiolipin biosynthesis partially suppresses the sensitivity of an Escherichia coli mutant lacking OmpC to envelope stress
Dae-Beom Ryu, Umji Choi, Gyubin Han, Chang-Ro Lee
Journal of Microbiology.2025; 63(11): e2507004. CrossRef
Identification of Genetic and Environmental Factors Suppressing the Lethality and Antibiotic Susceptibility Mediated by Depletion of LptD, a Lipopolysaccharide Transport Protein
Umji Choi, Ji Eun Son, Gyubin Han, Chang-Ro Lee
Journal of Microbiology and Biotechnology.2025;[Epub] CrossRef
PhoPQ-mediated lipopolysaccharide modification governs intrinsic resistance to tetracycline and glycylcycline antibiotics in Escherichia coli
Byoung Jun Choi, Umji Choi, Dae-Beom Ryu, Chang-Ro Lee, Mehrad Hamidian, You-Hee Cho
mSystems.2024;[Epub] CrossRef
Lytic transglycosylase repertoire diversity enables intrinsic antibiotic resistance and daughter cell separation in Escherichia coli under acidic stress
Ji Eun Son, Si Hyoung Park, Umji Choi, Chang-Ro Lee, Laurent Poirel
Antimicrobial Agents and Chemotherapy.2024;[Epub] CrossRef
Trans-cinnamaldehyde inhibits Escherichia coli growth by regulating lipopolysaccharide accumulation
Huanling Xing, Xiaomin Liu, Jianhao Lin, Mingfei Sun, Junyi Huang, Xinghai Li, Yanqun Li, Shining Guo, Fang Zhou, Hong Wu
Food Bioscience.2024; 61: 104559. CrossRef
Coordinated and Distinct Roles of Peptidoglycan Carboxypeptidases DacC and DacA in Cell Growth and Shape Maintenance under Stress Conditions
Umji Choi, Si Hyoung Park, Han Byeol Lee, Ji Eun Son, Chang-Ro Lee, Cristina Solano
Microbiology Spectrum.2023;[Epub] CrossRef
NoiD, a DedA membrane protein required for homeostasis maintaining of Rhizobium leguminosarum biovar viciae during symbiosis with Pisum sativum
Xiaofang Li, Jiaming Xu, Yajuan Wei, Zirui Chen
Symbiosis.2022; 86(1): 81. CrossRef
Conserved Tandem Arginines for PbgA/YejM Allow Salmonella Typhimurium To Regulate LpxC and Control Lipopolysaccharide Biogenesis during Infection
Nicole P. Giordano, Joshua A. Mettlach, Zachary D. Dalebroux, Manuela Raffatellu
Infection and Immunity.2022;[Epub] CrossRef
Divergent Effects of Peptidoglycan Carboxypeptidase DacA on Intrinsic β-Lactam and Vancomycin Resistance
Si Hyoung Park, Umji Choi, Su-Hyun Ryu, Han Byeol Lee, Jin-Won Lee, Chang-Ro Lee, Krisztina M. Papp-Wallace
Microbiology Spectrum.2022;[Epub] CrossRef
Cryo-EM structure of transmembrane AAA+ protease FtsH in the ADP state
Wu Liu, Martien Schoonen, Tong Wang, Sean McSweeney, Qun Liu
Communications Biology.2022;[Epub] CrossRef
Checkpoints That Regulate Balanced Biosynthesis of Lipopolysaccharide and Its Essentiality in Escherichia coli
Gracjana Klein, Alicja Wieczorek, Martyna Szuster, Satish Raina
International Journal of Molecular Sciences.2021; 23(1): 189. CrossRef

Phenotypic characterization of a conserved inner membrane protein YhcB in Escherichia coli: Chul Gi Sung , Umji Choi , Chang-Ro Lee; J. Microbiol. 2020;58(7):598-605. Published online April 22, 2020; DOI: https://doi.org/10.1007/s12275-020-0078-4

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Abstract PDF

Although bacteria have diverse membrane proteins, the function of many of them remains unknown or uncertain even in Escherichia coli. In this study, to investigate the function of hypothetical membrane proteins, genome-wide analysis of phenotypes of hypothetical membrane proteins was performed under various envelope stresses. Several genes responsible for adaptation to envelope stresses were identified. Among them, deletion of YhcB, a conserved inner membrane protein of unknown function, caused high sensitivities to various envelope stresses and increased membrane permeability, and caused growth defect under normal growth conditions. Furthermore, yhcB deletion resulted in morphological aberration, such as branched shape, and cell division defects, such as filamentous growth and the generation of chromosome- less cells. The analysis of antibiotic susceptibility showed that the yhcB mutant was highly susceptible to various anti-folate antibiotics. Notably, all phenotypes of the yhcB mutant were completely or significantly restored by YhcB without the transmembrane domain, indicating that the localization of YhcB on the inner membrane is dispensable for its function. Taken together, our results demonstrate that YhcB is involved in cell morphology and cell division in a membrane localization-independent manner.

Citations

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YhcB mediates growth-phase control of fatty acid biosynthesis through regulation of acetyl-CoA carboxylase
Hannah M. Stanley, M. Stephen Trent, K. Heran Darwin
mBio.2026;[Epub] CrossRef
Inhibition of cardiolipin biosynthesis partially suppresses the sensitivity of an Escherichia coli mutant lacking OmpC to envelope stress
Dae-Beom Ryu, Umji Choi, Gyubin Han, Chang-Ro Lee
Journal of Microbiology.2025; 63(11): e2507004. CrossRef
Identification of Genetic and Environmental Factors Suppressing the Lethality and Antibiotic Susceptibility Mediated by Depletion of LptD, a Lipopolysaccharide Transport Protein
Umji Choi, Ji Eun Son, Gyubin Han, Chang-Ro Lee
Journal of Microbiology and Biotechnology.2025;[Epub] CrossRef
Co-ordinated assembly of the multilayered cell envelope of Gram-negative bacteria
Elayne M Fivenson, Laurent Dubois, Thomas G Bernhardt
Current Opinion in Microbiology.2024; 79: 102479. CrossRef
Loss of YhcB results in overactive fatty acid biosynthesis
Hannah M. Stanley, M. Stephen Trent, K. Heran Darwin
mBio.2024;[Epub] CrossRef
A New Factor LapD Is Required for the Regulation of LpxC Amounts and Lipopolysaccharide Trafficking
Alicja Wieczorek, Anna Sendobra, Akshey Maniyeri, Magdalena Sugalska, Gracjana Klein, Satish Raina
International Journal of Molecular Sciences.2022; 23(17): 9706. CrossRef
Loss of YhcB results in dysregulation of coordinated peptidoglycan, LPS and phospholipid synthesis during Escherichia coli cell growth
Emily C. A. Goodall, Georgia L. Isom, Jessica L. Rooke, Karthik Pullela, Christopher Icke, Zihao Yang, Gabriela Boelter, Alun Jones, Isabel Warner, Rochelle Da Costa, Bing Zhang, James Rae, Wee Boon Tan, Matthias Winkle, Antoine Delhaye, Eva Heinz, Jean-F
PLOS Genetics.2021; 17(12): e1009586. CrossRef
The inner membrane protein LapB is required for adaptation to cold stress in an LpxC-independent manner
Han Byeol Lee, Si Hyoung Park, Chang-Ro Lee
Journal of Microbiology.2021; 59(7): 666. CrossRef

Protocol

Determination of protein phosphorylation by polyacrylamide gel electrophoresis: Chang-Ro Lee , Young-Ha Park , Huitae Min , Yeon-Ran Kim , Yeong-Jae Seok; J. Microbiol. 2019;57(2):93-100. Published online January 31, 2019; DOI: https://doi.org/10.1007/s12275-019-9021-y

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Abstract PDF

Phosphorylation is the most important modification for protein regulation; it controls many signal transduction pathways in all organisms. While several tools to detect phosphorylated proteins have been developed to study a variety of basic cellular processes involving protein phosphorylation, these methods have several limitations. Many proteins exhibit a phosphorylation-dependent electrophoretic mobility shift (PDEMS) in sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE), and the molecular mechanism responsible for this phenomenon has been elucidated recently. The method for detecting phosphorylated proteins can be simplified by the application of the PDEMS. Herein, we present a novel simple method to detect protein phosphorylation, which is based on the construction of a variant protein displaying a PDEMS. The PDEMS of proteins is caused by the distribution of negatively charged amino acids around the phosphorylation site, i.e. an electrophoretic mobility shift (EMS)-related motif (ΘX1-3ΘX1-3Θ, where Θ corresponds to an acidic or phosphorylated amino acid and X represents any amino acid). The EMS-related motif can be constructed by the introduction of a negative charge by phosphorylation; it results in the decreased binding of SDS to the proteins, consequently inducing the retardation of the mobility of the protein during SDS-PAGE. Based on these molecular analyses of the PDEMS, a protein with the EMSrelated motif is designed and used to determine the in vivo phosphorylation state of the protein. This method may be used as a general strategy to easily measure the ratio of protein phosphorylation in cells.

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Article

Molecular characterization of SCO0765 as a cellotriose releasing endo-β-1,4-cellulase from Streptomyces coelicolor A(3): Joo-Bin Hong , Vijayalakshmi Dhakshnamoorthy , Chang-Ro Lee; J. Microbiol. 2016;54(9):626-631. Published online August 31, 2016; DOI: https://doi.org/10.1007/s12275-016-6271-9

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Abstract PDF

The sco0765 gene was annotated as a glycosyl hydrolase family 5 endoglucanase from the genomic sequence of Streptomyces coelicolor A3(2) and consisted of 2,241 bp encoding a polypeptide of 747 amino acids (molecular weight of 80.5 kDa) with a 29-amino acid signal peptide for secretion. The SCO0765 recombinant protein was heterogeneously overexpressed in Streptomyces lividans TK24 under the control of a strong ermE* promoter. The purified SCO0765 protein showed the expected molecular weight of the mature form (718 aa, 77.6 kDa) on sodium dodecyl sulfate-polyacryl amide gel electrophoresis. SCO0765 showed high activity toward β-glucan and carboxymethyl cellulose (CMC) and negligible activity to Avicel, xylan, and xyloglucan. The SCO0765 cellulase had a maximum activity at pH 6.0 and 40°C toward CMC and at pH 9.0 and 50–60°C toward β-glucan. Thin layer chromatography of the hydrolyzed products of CMC and β-glucan by SCO0765 gave cellotriose as the major product and cellotetraose, cellopentaose, and longer oligosaccharides as the minor products. These results clearly demonstrate that SCO0765 is an endo-β-1,4-cellulase, hydrolyzing the β-1,4 glycosidic bond of cellulose into cellotriose.

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Cellulase Promotes Mycobacterial Biofilm Dispersal in Response to a Decrease in the Bacterial Metabolite Gamma-Aminobutyric Acid
Jiaqi Zhang, Yingying Liu, Junxing Hu, Guangxian Leng, Xining Liu, Zailin Cui, Wenzhen Wang, Yufang Ma, Shanshan Sha
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