Journal of Microbiology

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Encapsulin protein MAV2054 enhances Mycobacterium avium virulence by promoting Cdc42-dependent epithelial cell invasion: Dong Ho Kim, I Jeong Jo, Min Ju Kang, Yi Seol Kim, Duyen Do Tran Huong, Kyungho Woo, Ho-Sung Park, Hwa-Jung Kim, Chul Hee Choi; J. Microbiol. 2025;63(11):e2506008. Published online November 30, 2025; DOI: https://doi.org/10.71150/jm.2506008

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Abstract PDF: Mycobacterium avium complex (MAC) organisms are widespread environmental pathogens associated with chronic pulmonary infections. Although M. avium is known to invade epithelial cells, the molecular mechanisms underlying this process remain incompletely understood. In this study, we identified a novel role for MAVRS09815 (formerly MAV2054), a family 2A encapsulin nanocompartment shell protein, in mediating bacterial adhesion, epithelial cell invasion, and in vivo virulence. We engineered a recombinant M. smegmatis strain expressing MAV2054 (Ms_2054) and an M. avium MAV2054 deletion mutant (Δ2054). Ms_2054 exhibited enhanced epithelial invasion, whereas Δ2054 showed reduced intracellular survival. Recombinant MAV2054 protein was bound directly to human epithelial cells in a dose-dependent manner. Pretreatment of host cells with cytochalasin D or vinblastine significantly inhibited bacterial internalization, indicating that MAV2054-mediated invasion is cytoskeleton-dependent. Confocal and scanning electron microscopy revealed MAV2054-dependent membrane rearrangements during infection. Pull-down assays demonstrated that MAV2054 activates Cdc42, a key regulator of actin polymerization, with reduced activation observed in Δ2054-infected cells. In a murine intratracheal infection model, the Δ2054 exhibited significantly reduced bacterial burdens and lung inflammation compared to the wild type. These findings demonstrate that MAV2054 enhances M. avium virulence by promoting epithelial cell invasion through Cdc42-dependent cytoskeletal remodeling. This study reveals a previously unrecognized role for an encapsulin-like protein in host-pathogen interactions and highlights its potential as a therapeutic target in MAC infections.

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The osmotic stress response operon betIBA is under the functional regulation of BetI and the quorum-sensing regulator AnoR in Acinetobacter nosocomialis: Bindu Subhadra , Surya Surendran , Bo Ra Lim , Jong Sung Yim , Dong Ho Kim , Kyungho Woo , Hwa-Jung Kim , Man Hwan Oh , Chul Hee Choi; J. Microbiol. 2020;58(6):519-529. Published online May 27, 2020; DOI: https://doi.org/10.1007/s12275-020-0186-1

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Adaptation to changing environmental conditions is crucial for the survival of microorganisms. Bacteria have evolved various mechanisms to cope with osmotic stress. Here, we report the identification and functional characterization of the osmotic stress response operon, betIBA, in Acinetobacter nosocomialis. The betIBA operon encodes enzymes that are important for the conversion of choline to the osmoprotectant, glycine betaine. The betIBA operon is polycistronic and is under the regulation of the first gene, betI, of the same operon. A bioinformatics analysis revealed the presence of a BetI-binding motif upstream of the betIBA operon, and electrophoretic mobility shift assays confirmed the specific binding of BetI. An mRNA expression analysis revealed that expression of betI, betB, and betA genes is elevated in a betIeletion mutant compared with the wild type, confirming that the autorepressor BetI represses the betIBA operon in A. nosocomialis. We further found that the betIBA operon is under the transcriptional control of the quorum-sensing (QS) regulator, AnoR in, A. nosocomialis. A subsequent analysis of the impact of BetI on expression of the QS genes, anoR and anoI, demonstrated that BetI acts as a repressor of anoR and anoI. In addition, it was noticed that the osmotic stress response regulator, OmpR might play an important role in controlling the expression of betIBA operon in A. nosocomialis. Collectively, these data demonstrate that QS and osmotic stress-response systems are correlated in A. nosocomialis and that the expression of genes in both systems is finely tuned by various feedback loops depending on osmolarity conditions.

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Regulation of the AcrAB efflux system by the quorum-sensing regulator AnoR in Acinetobacter nosocomialis: Bindu Subhadra , Surya Surendran , Bo Ra Lim , Jong Sung Yim , Dong Ho Kim , Kyungho Woo , Hwa-Jung Kim , Man Hwan Oh , Chul Hee Choi; J. Microbiol. 2020;58(6):507-518. Published online May 27, 2020; DOI: https://doi.org/10.1007/s12275-020-0185-2

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Abstract PDF

Multidrug efflux pumps play an important role in antimicrobial resistance and pathogenicity in bacteria. Here, we report the functional characterization of the RND (resistance-nodulation- division) efflux pump, AcrAB, in Acinetobacter nosocomialis. An in silico analysis revealed that homologues of the AcrAB efflux pump, comprising AcrA and AcrB, are widely distributed among different bacterial species. Deletion of acrA and/or acrB genes led to decreased biofilm/pellicle formation and reduced antimicrobial resistance in A. nosocomialis. RNA sequencing and mRNA expression analyses showed that expression of acrA/B was downregulated in a quorum sensing (QS) regulator (anoR)-deletion mutant, indicating transcriptional activation of the acrAB operon by AnoR in A. nosocomialis. Bioassays showed that secretion of N-acyl homoserine lactones (AHLs) was unaffected in acrA and acrB deletion mutants; however, AHL secretion was limited in a deletion mutant of acrR, encoding the acrAB regulator, AcrR. An in silico analysis indicated the presence of AcrR-binding motifs in promoter regions of anoI (encoding AHL synthase) and anoR. Specific binding of AcrR was confirmed by electrophoretic mobility shift assays, which revealed that AcrR binds to positions -214 and -217 bp upstream of the translational start sites of anoI and anoR, respectively, demonstrating transcriptional regulation of these QS genes by AcrR. The current study further addresses the possibility that AcrAB is controlled by the osmotic stress regulator, OmpR, in A. nosocomialis. Our data demonstrate that the AcrAB efflux pump plays a crucial role in biofilm/pellicle formation and antimicrobial resistance in A. nosocomialis, and is under the transcriptional control of a number of regulators. In addition, the study emphasizes the interrelationship of QS and AcrAB efflux systems in A. nosocomialis.

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Types and Mechanisms of Efflux Pump Systems and the Potential of Efflux Pump Inhibitors in the Restoration of Antimicrobial Susceptibility, with a Special Reference to Acinetobacter baumannii
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Journal Article

Zur-regulated lipoprotein A contributes to the fitness of Acinetobacter baumannii: Eun Kyung Lee , Chul Hee Choi , Man Hwan Oh; J. Microbiol. 2020;58(1):67-77. Published online January 2, 2020; DOI: https://doi.org/10.1007/s12275-020-9531-7

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Abstract PDF

Acinetobacter baumannii is a notorious nosocomial pathogen that commonly infects severely ill patients. Zinc (Zn) is essential to survive and adapt to different environment and host niches in A. baumannii. Of the Zinc uptake regulator (Zur)-regulated genes in A. baumannii, the A1S_3412 gene encoding a Zur-regulated lipoprotein A (ZrlA) is critical for cell envelope integrity and overcoming antibiotic exposure. This study investigated whether ZrlA contributes to the fitness of A. baumannii in vitro and in vivo using the wildtype A. baumannii ATCC 17978, ΔzrlA mutant, and zrlAcomplemented strains. The ΔzrlA mutant showed reduced biofilm formation, surface motility, and adherence to and invasion of epithelial cells compared to the wild-type strain. In a mouse pneumonia model, the ΔzrlA mutant showed significantly lower bacterial numbers in the blood than the wildtype strain. These virulence traits were restored in the zrlAcomplemented strain. Under static conditions, the expression of csuCDE, which are involved in the chaperone-usher pili assembly system, was significantly lower in the ΔzrlA mutant than in the wild-type strain. Moreover, the expression of the bfmR/S genes, which regulate the CsuA/BABCDE system, was significantly lower in the ΔzrlA mutant under static conditions than in the wild-type strain. Our results indicate that the zrlA gene plays a role in the fitness of A. baumannii by regulating the BfmR/S two-component system and subsequently the CsuA/BABCDE chaperone-usher pili assembly system, suggesting it as a potential target for anti-virulence strategies against A. baumannii.

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AbOmpA in Acinetobacter baumannii: exploring virulence mechanisms of outer membrane-integrated and outer membrane vesicle-associated AbOmpA and developing anti-infective agents targeting AbOmpA
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Research Support, Non-U.S. Gov'ts

Acinetobacter baumannii Outer Membrane Protein A Modulates the Biogenesis of Outer Membrane Vesicles: Dong Chan Moon , Chul Hee Choi , Jung Hwa Lee , Chi-Won Choi , Hye-Yeon Kim , Jeong Soon Park , Seung Il Kim , Je Chul Lee; J. Microbiol. 2012;50(1):155-160. Published online February 27, 2012; DOI: https://doi.org/10.1007/s12275-012-1589-4

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Abstract PDF

Acinetobacter baumannii secretes outer membrane vesicles (OMVs) during both in vitro and in vivo growth, but the biogenesis mechanism by which A. baumannii produces OMVs remains undefined. Outer membrane protein A of A. baumannii (AbOmpA) is a major protein in the outer membrane and the C-terminus of AbOmpA interacts with diaminopimelate of peptidoglycan. This study investigated the role of AbOmpA in the biogenesis of A. baumannii OMVs. Quantitative and qualitative approaches were used to analyze OMV biogenesis in A. baumannii ATCC 19606T and an isogenic ΔAbOmpA mutant. OMV production was significantly increased in the ΔAbOmpA mutant compared to wild-type bacteria as demonstrated by quantitation of proteins and lipopolysaccharides (LPS) packaged in OMVs. LPS profiles prepared from OMVs from wild-type bacteria and the ΔAbOmpA mutant had identical patterns, but proteomic analysis showed different protein constituents in OMVs from wild-type bacteria compared to the ΔAbOmpA mutant. In conclusion, AbOmpA influences OMV biogenesis by controlling OMV production and protein composition.

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Acinetobacter baumannii Outer Membrane Protein A Induces Dendritic Cell Death Through Mitochondrial Targeting: Jun Sik Lee , Chul Hee Choi , Jung Wook Kim , Je Chul Lee; J. Microbiol. 2010;48(3):387-392. Published online June 23, 2010; DOI: https://doi.org/10.1007/s12275-010-0155-1

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Abstract PDF

Acinetobacter baumannii outer membrane protein A (AbOmpA) is a potential virulence factor that induces epithelial cell death, but its pathologic effects on the immune system have yet to be determined. The present study investigated the pathologic events occurring in dendritic cells (DCs) exposed to a cytotoxic concentration of AbOmpA. AbOmpA induced early-onset apoptosis and delayed-onset necrosis in DCs. AbOmpA targeted the mitochondria and induced the production of reactive oxygen species (ROS). ROS were directly responsible for both apoptosis and necrosis of AbOmpA-treated DCs. These results demonstrate that the AbOmpA secreted from A. baumannii induces DC death, which may impair T cell biology to induce adaptive immune responses against A. baumannii.

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Anti-Tumor Activity of Acinetobacter baumannii Outer Membrane Protein A on Dendritic Cell-Based Immunotherapy against Murine Melanoma: Jun Sik Lee , Jung Wook Kim , Chul Hee Choi , Won Kee Lee , Hae Young Chung , Je Chul Lee; J. Microbiol. 2008;46(2):221-227. Published online June 11, 2008; DOI: https://doi.org/10.1007/s12275-008-0052-z

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Abstract PDF

Acinetobacter baumannii outer membrane protein A (AbOmpA) is a major surface protein that is an important pathogen-associated molecular pattern. Based on our previous findings that AbOmpA induced the phenotypic maturation of dendritic cells (DCs) and drove the Th1 immune response in vitro, we investigated the therapeutic efficacy of AbOmpA-pulsed DC vaccines in a murine melanoma model. The surface expression of co-stimulatory molecules (CD80 and CD86) and major histocompatibility complex class I and II molecules was higher in DCs pulsed with AbOmpA alone or with a combination of B16F10 cell lysates than that of DCs pulsed with B16F10 cell lysates. AbOmpA stimulated the maturation of murine splenic DCs in vivo. In a therapeutic model of murine melanoma, AbOmpA-pulsed DCs significantly retarded tumor growth and improved the survival of tumor-bearing mice. AbOmpA-pulsed DCs significantly enhanced CD8+, interleukin-2+ T cells and CD4+, interferon-γ+ T cells in tumor-bearing mice. These results provide evidence that AbOmpA may be therapeutically useful in adjuvant DC immunotherapy against poorly immunogenic melanoma without tumor-specific antigens.

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