Journal of Microbiology

Research article

Genomic signatures associated with epidemiologically defined high-risk pathogenic Escherichia coli isolates identified by interpretable machine learning: Yoojung Hwang, Woo Young Cho, Woojung Lee, Insun Joo, Jeong-Ih Shin, Mi-Ran Seo, Seung-Hun Shin, Kwan Soo Ko, Kun Taek Park, Yeun-Jun Chung, Seung-Hyun Jung; J. Microbiol. 2026;64(8):e2604011. Published online August 31, 2026; DOI: https://doi.org/10.71150/jm.2604011

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Abstract PDF Supplementary Material: Pathogenic Escherichia coli is a major cause of foodborne illness worldwide and includes strains capable of causing severe disease. To establish a genome-informed framework for foodborne outbreak surveillance, we analyzed 1,029 E. coli isolates from clinical, food, livestock, and environmental sources using whole-genome sequencing. Pathogenic isolates obtained from human clinical cases or linked to documented outbreaks were classified as epidemiologically defined high-risk (EpiHR), whereas the remaining pathogenic isolates were classified as non-EpiHR. Virulence-associated genomic features were extracted using a bioinformatics pipeline, and four machine learning (ML) algorithms, including gradient boosting machine, random forest (RF), and support vector machines with linear and radial basis function kernels, were evaluated. Among them, the RF model showed the best performance, achieving an area under the curve (AUC) of 0.98 and accuracy of 0.93 in 10-fold cross-validation. Additional leave-one-group-out validation showed retained discrimination across held-out sequence types and serotypes, although performance was reduced when isolates were grouped by isolation source. Evaluation using an independent test dataset of 1,908 publicly available pathogenic E. coli genomes showed an AUC of 0.97 and a sensitivity of 0.98. Feature importance analysis using Shapley additive explanations identified influential predictive features, including traT, etpB, and enterotoxin-associated genes. A reduced 10-feature model achieved an AUC of 0.79 in the independent test dataset, supporting its exploratory use for future simplified screening approaches. These results indicate that genome-based ML provides a sensitive framework for surveillance-oriented prioritization of EpiHR pathogenic E. coli isolates, with model predictions interpreted together with epidemiological information.

Article

Comparative analysis of the colistin resistance-regulating gene cluster in Klebsiella species: Sun Ju Kim , Hongbaek Cho , Kwan Soo Ko; J. Microbiol. 2022;60(5):461-468. Published online April 18, 2022; DOI: https://doi.org/10.1007/s12275-022-1640-z

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CrrAB two-component regulatory system is associated with colistin resistance in Klebsiella pneumoniae. Recently, some K. pneumoniae isolates lacking crrAB genes have been identified. In this study, we investigated the distribution and structural variation of the crrBAC-kexD cluster. To evaluate the structural variation of the crrBAC-kexD cluster, we explored 59 clinical K. pneumoniae isolates from Korea, and 508 whole genomes of K. pneumoniae and other strains of Klebsiella sp. Significant structural variations in crrBAC-kexD and its surrounding regions were identified among K. pneumoniae genomes. Within the genus Klebsiella, the cluster was identified only in K. pneumoniae, K. variicola, and K. quasipneumoniae, which form the K. pneumoniae complex. Among the 304 available K. pneumoniae genomes, an intact crrBAC-kexD cluster was identified in 178 isolates (58.6%), while the cluster was absent in 90 isolates (29.6%). Partial deletions within the cluster were identified in 22 genomes (7.2%). The most diverse structural patterns of the crrBAC-kexD cluster were observed in ST11 strains. Some clades lacked the crrBAC-kexD cluster. The crrBAC-kexD cluster was identified in the genomes of other bacterial species, including Citrobacter freundii and Enterobacter ludwigii. The crrBAC-kexD cluster is proposed to have been acquired by the ancestor of the K. pneumoniae complex from other bacterial species and the cluster may have been lost and re-acquired repeatedly in K. pneumoniae strains according to the phylogenetic analysis. The dynamic evolution of the crrBAC-kexD cluster suggests that it may have other roles, in addition to colistin resistance, in bacterial physiology.

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Antibiotic Resistance in Klebsiella pneumoniae and Related Enterobacterales: Molecular Mechanisms, Mobile Elements, and Therapeutic Challenges
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Genevieve S. Dobihal, Kristen Lewis, Tian Huai Shen, Carmen M. Herrera, Lisa Yu, Jonathan Barasch, M. Stephen Trent, Josué Flores-Kim, Anne-Catrin Uhlemann
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High prevalence of polymyxin-heteroresistant carbapenem-resistant Klebsiella pneumoniae and its within-host evolution to resistance among critically ill scenarios
Xiaoli Wang, Tianjiao Meng, Yunqi Dai, Hong-Yu Ou, Meng Wang, Bin Tang, Jingyong Sun, Decui Cheng, Tingting Pan, Ruoming Tan, Hongping Qu
Infection.2025; 53(1): 271. CrossRef
Roles of crrAB two-component regulatory system in Klebsiella pneumoniae: growth yield, survival in initial colistin treatment stage, and virulence
Sun Ju Kim, Jong Hyun Shin, Hyunkeun Kim, Kwan Soo Ko
International Journal of Antimicrobial Agents.2024; 63(1): 107011. CrossRef
Role of efflux pumps, their inhibitors, and regulators in colistin resistance
Yinhuan Ding, Jingchen Hao, Weijia Xiao, Caihong Ye, Xue Xiao, Chunxia Jian, Min Tang, Guangrong Li, Jinbo Liu, Zhangrui Zeng
Frontiers in Microbiology.2023;[Epub] CrossRef

Article

Detection of colistin-resistant populations prior to antibiotic exposure in KPC-2-producing Klebsiella pneumoniae clinical isolates: Jungyu Seo , Yu Mi Wi , Jong Min Kim , Yae-Jean Kim , Kwan Soo Ko; J. Microbiol. 2021;59(6):590-597. Published online March 29, 2021; DOI: https://doi.org/10.1007/s12275-021-0610-1

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Abstract PDF

Although colistin is frequently regarded as the antibiotic of last resort in treating carbapenem-resistant Klebsiella pneumoniae, colistin heteroresistance may in part be associated with antibiotic treatment failure. However, we do not know how widespread the colistin heteroresistance is in carbapenem- resistant K. pneumoniae isolates. In this study, we performed colistin disc diffusion assays, E-tests, and population analysis profiling for KPC-2-producing K. pneumoniae isolates to identify colistin heteroresistance. Although no colistin- resistant colonies were detected by the disc diffusion test and E-test, a colistin-resistant subpopulation was identified in population analysis profiling in all colistin-susceptible, KPC-2-producing K. pneumoniae isolates. Colistin-resistant subpopulations were also identified even when isolates had no colistin exposure. The ratio of colistin-resistant subpopulations to the total population increased as the exposure concentration of colistin increased. In in vitro time-kill assays, regrowth was observed in all isolates after 2 h upon exposure to colistin. We identified common amino acid alterations in PhoQ, PhoP, and PmrB in colistin-resistant subpopulations from some isolates, but no substitutions were found in most resistant subpopulations from other isolates. In all colistin-resistant subpopulations, overexpression of PhoQ and PbgP was observed. In this study, we demonstrated that colistin heteroresistance may be common in KPC-2-producing K. pneumoniae isolates, which could not be detected in the disc diffusion method and E-test. Colistin heteroresistance may cause colistin treatment failure in part and may evolve into resistance. Thus, development of more reliable diagnostic methods is required to detect colistin heteroresistance.

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High prevalence of polymyxin-heteroresistant carbapenem-resistant Klebsiella pneumoniae and its within-host evolution to resistance among critically ill scenarios
Xiaoli Wang, Tianjiao Meng, Yunqi Dai, Hong-Yu Ou, Meng Wang, Bin Tang, Jingyong Sun, Decui Cheng, Tingting Pan, Ruoming Tan, Hongping Qu
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Qihong Kuang, Xiaorui Zhang, Fangping Ou, Lingling Liu, Hui Deng, Bo Yang, Lingxian Yi, Daojin Yu
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Development of colistin resistance via heteroresistance modeling in Klebsiella pneumoniae: A diagnostic study
Jungyu Seo, Kwan Soo Ko
Precision and Future Medicine.2024; 8(1): 10. CrossRef
Conversion to colistin susceptibility by tigecycline exposure in colistin-resistant Klebsiella pneumoniae and its implications to combination therapy
Suyeon Park, Jihyun Choi, Dongwoo Shin, Ki Tae Kwon, Si-Ho Kim, Yu Mi Wi, Kwan Soo Ko
International Journal of Antimicrobial Agents.2024; 63(1): 107017. CrossRef
Insight into Antibiotic Synergy Combinations for Eliminating Colistin Heteroresistant Klebsiella pneumoniae
Sahaya Glingston Rajakani, Basil Britto Xavier, Adwoa Sey, El Bounja Mariem, Christine Lammens, Herman Goossens, Youri Glupczynski, Surbhi Malhotra-Kumar
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Heteroresistance Is Associated With in vitro Regrowth During Colistin Treatment in Carbapenem-Resistant Klebsiella pneumoniae
Yifan Wang, Xinqian Ma, Lili Zhao, Yukun He, Wenyi Yu, Shining Fu, Wentao Ni, Zhancheng Gao
Frontiers in Microbiology.2022;[Epub] CrossRef
Prevalence of Mutated Colistin-Resistant Klebsiella pneumoniae: A Systematic Review and Meta-Analysis
Nik Yusnoraini Yusof, Nur Iffah Izzati Norazzman, Siti Nur’ain Warddah Ab Hakim, Mawaddah Mohd Azlan, Amy Amilda Anthony, Fatin Hamimi Mustafa, Naveed Ahmed, Ali A. Rabaan, Souad A. Almuthree, Abdulsalam Alawfi, Amer Alshengeti, Sara Alwarthan, Mohammed G
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Retraction

Cryptic prophages in a blaNDM-1-bearing plasmid increase bacterial survival against high NaCl concentration, high and low temperatures, and oxidative and immunological stressors: So Yeon Kim , Kwan Soo Ko; J. Microbiol. 2020;58(6):483-488. Published online March 28, 2020; DOI: https://doi.org/10.1007/s12275-020-9605-6

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Abstract PDF

In this study, we investigated the effect of cryptic prophage regions in a blaNDM-1-bearing plasmid, which was identified in a patient from South Korea, on the survival of bacteria against adverse environmental conditions. First, we conjugated the intact plasmid and plasmids with deleted cryptic prophages into Escherichia coli DH5α. The E. coli transconjugants carrying the plasmid with intact cryptic prophages showed increased survival during treatment with a high concentration of NaCl, high and low temperatures, an oxidative stressor (H2O2), and an immunological stressor (human serum). By contrast, the transconjugants carrying the plasmid with a single-cryptic prophage knockout did not show any change in survival rates. mRNA expression analyses revealed that the genes encoding sigma factor proteins were highly upregulated by the tested stressors and affected the expression of various proteins (antioxidant, cell osmosis-related, heat shock, cold shock, and universal stress proteins) associated with the specific defense against each stress. These findings indicate that a bacterial strain carrying a plasmid with intact carbapenemase gene and cryptic prophage regions exhibited an increased resistance against simulated environmental stresses, and cryptic prophages in the plasmid might contribute to this enhanced stress resistance. Our study indicated that the coselection of antibiotic resistance and resistance to other stresses may help bacteria to increase survival rates against adverse environments and disseminate.

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Article

Rapid determination of carbapenem resistance by low-cost colorimetric methods: Propidium Iodide and alamar blue staining: Jiyoon Choi , Jiwon Baek , Daehyuk Kweon , Kwan Soo Ko , Hyunjin Yoon; J. Microbiol. 2020;58(5):415-421. Published online March 28, 2020; DOI: https://doi.org/10.1007/s12275-020-9549-x

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Abstract PDF

Carbapenems are a class of β-lactam antibiotics with a broad antimicrobial activity spectrum. Owing to their sturdy structures resistant to most β-lactamases, they have been regarded as one of the last-resort antibiotics for combating multidrugresistant bacterial infections. However, the emergence of carbapenem resistance increases predominantly in nosocomial pathogens. To prevent spread of carbapenem resistance in early stages, it is imperative to develop rapid diagnostic tests that will substantially reduce the time and cost in determining carbapenem resistance. Thus, we devised a staining-based diagnostic method applicable to three different Gram-negative pathogens of Acinetobacter baumannii, Escherichia coli, and Klebsiella pneumoniae, all with the high potential to develop carbapenem resistance. Regardless of the resistance mechanisms presented by bacterial species and strains, double staining with propidium iodide (PI) and alamar blue (AB) identified resistant bacteria with an average sensitivity of 95.35%, 7 h after imipenem treatments in 343 clinical isolates. Among the three species tested, A. baumannii showed the highest diagnostic sensitivity of 98.46%. The PI and ABmediated staining method could be a promising diagnostic
method
with high-throughput efficacy and low cost.

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Review

Antibiotic-resistant clones in Gram-negative pathogens: presence of global clones in Korea: Kwan Soo Ko; J. Microbiol. 2019;57(3):195-202. Published online October 2, 2018; DOI: https://doi.org/10.1007/s12275-019-8491-2

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Abstract PDF

Antibiotic resistance is a global concern in public health. Antibiotic-resistant clones can spread nationally, internationally, and globally. This review considers representative antibiotic-resistant Gram-negative bacterial clones–CTX-M- 15-producing ST131 in Escherichia coli, extended-spectrum β-lactamase-producing ST11 and KPC-producing ST258 in Klebsiella pneumoniae, IMP-6-producing, carbapenem-resistant ST235 in Pseudomonas aeruginosa, and OXA-23- producing global clone 2 in Acinetobacter baumannii–that have disseminated worldwide, including in Korea. The findings highlight the urgency for systematic monitoring and international cooperation to suppress the emergence and propagation of antibiotic resistance.

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Article

Comparison of virulence between matt and mucoid colonies of Klebsiella pneumoniae coproducing NDM-1 and OXA-232 isolated from a single patient: Haejeong Lee , Jin Yang Baek , So Yeon Kim , HyunJi Jo , KyeongJin Kang , Jae-Hoon Ko , Sun Young Cho , Doo Ryeon Chung , Kyong Ran Peck , Jae-Hoon Song , Kwan Soo Ko; J. Microbiol. 2018;56(9):665-672. Published online August 23, 2018; DOI: https://doi.org/10.1007/s12275-018-8130-3

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Abstract PDF

Nine Klebsiella pneumoniae isolates coproducing NDM-1 and OXA-232 carbapenemases were successively isolated from a single patient. Although they were isolated simultaneously and were isogenic, they presented different colony phenotypes (matt and mucoid). All nine isolates were resistant to most antibiotics except colistin and fosfomycin. In addition, matt-type isolates were resistant to tigecycline. No differences were detected in the cps cluster sequences, except for the insertion of IS5 in the wzb gene of two matt-type isolates. In vitro virulence assays based on production of capsular polysaccharide, biofilm formation, and resistance to human serum indicated that the mucoid-type isolates were significantly more virulent than the matt-type. In addition, mucoid-type isolates showed higher survival rates than the matt-type ones in infection experiments in the fruit fly, suggesting a higher virulence of K. pneumoniae isolates with a mucoid phenotype. To our knowledge, this is the first report of K. pneumoniae colonies with different phenotypes being isolated from the same sample. In addition, we show that virulence varies with colony phenotype. Dissemination of K. pneumoniae isolates expressing both antibiotic resistance and high virulence would constitute a great threat.

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Roles of crrAB two-component regulatory system in Klebsiella pneumoniae: growth yield, survival in initial colistin treatment stage, and virulence
Sun Ju Kim, Jong Hyun Shin, Hyunkeun Kim, Kwan Soo Ko
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Article

Colistin resistance in Enterobacter spp. isolates in Korea: Yoon-Kyoung Hong , Ji-Young Lee , Kwan Soo Ko; J. Microbiol. 2018;56(6):435-440. Published online June 1, 2018; DOI: https://doi.org/10.1007/s12275-018-7449-0

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Abstract PDF

We investigated the colistin resistance rate among 356 Enterobacter spp. clinical isolates from eight hospitals in Korea. Antibiotic susceptibility testing was performed by broth microdilution. While 51 of 213 (23.9%) Enterobacter cloacae isolates were colistin-resistant, only six of 143 (4.2%) E. aerogenes isolates showed resistance. We also identified the skip well phenotype in eight E. cloacae and three E. aerogenes isolates. Multilocus sequence typing for E. cloacae and randomly amplified polymorphic DNA analysis and enterobacterial repetitive intergenic consensus PCR for E. aerogenes revealed that clonal spreading of colistin-resistant and skip well Enterobacter spp. isolates had not occurred. In vitro time-kill assays were performed with three colistin-resistant, three skip well, and two colistin-susceptible isolates of E. cloacae and E. aerogenes. Inconsistent results were observed among isolates with skip well phenotypes; while some were eradicated by 2 mg/L colistin, others were not. This suggests that skip well isolates have differentiated into different categories. As the high rates of colistin resistance in E. cloacae detected are of clinical concern, continuous monitoring is warranted. In addition, the clinical implications and mechanisms of the skip well phenotype should be investigated to ensure the appropriate use of colistin against Enterobacter infections.

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Article

Imipenem-resistant Gram-negative bacterial isolates carried by persons upon medical examination in Korea: So Yeon Kim , Sang Yop Shin , Ji-Young Rhee , Kwan Soo Ko; J. Microbiol. 2017;55(8):612-618. Published online July 18, 2017; DOI: https://doi.org/10.1007/s12275-017-6555-8

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Carbapenem-resistant Gram-negative bacteria (CR-GNB) have emerged and disseminated worldwide, become a great concern worldwide including Korea. The prevalence of fecal carriage of imipenem-resistant Gram-negative bacteria (IRGNB) in persons in Korea was investigated. Stool samples were collected from 300 persons upon medical examination. Samples were screened for IR-GNB by using MacConkey agar with 2 μl/ml imipenem. Species were identified by 16S rRNA gene sequence analysis, and antimicrobial susceptibility was determined by the broth microdilution method. In total, 82 IR-GNB bacterial isolates were obtained from 79 (26.3%) out of 300 healthy persons. Multilocus sequence typing analysis showed very high diversity among IR P. aeruginosa, S. maltophilia, and E. cloacae isolates, and pulsedfield gel electrophoresis revealed five main pulsotypes of IR P. mirabilis. As for the presence of metallo-β-lactamases (MBLs), only one IMP-25-producing S. marcescens isolate was identified. Although only one carbapenemase-producing isolate was identified, the high colonization rates with IRGNB isolates in this study is notable because carriers may be a reservoir for the dissemination of resistant pathogens within the community as well as in health care institutions.

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Global mapping of antibiotic resistance rates among clinical isolates of Stenotrophomonas maltophilia: a systematic review and meta-analysis
Narjess Bostanghadiri, Mohammad Sholeh, Tahereh Navidifar, Leila Dadgar-Zankbar, Zahra Elahi, Alex van Belkum, Davood Darban-Sarokhalil
Annals of Clinical Microbiology and Antimicrobials.2024;[Epub] CrossRef
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Joanna S. Brooke
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So Yeon Kim, Jungyu Seo, Juyoun Shin, Yeun-Jun Chung, In Young Jeon, Seon Jin Yun, Yeon-Sook Kim, Kwan Soo Ko
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Article

Characteristics of the community-genotype sequence type 72 methicillin-resistant Staphylococcus aureus isolates that underlie their persistence in hospitals: Eun-Jeong Joo , Ji-Young Choi , Doo Ryeon Chung , Jae-Hoon Song , Kwan Soo Ko; J. Microbiol. 2016;54(6):445-450. Published online May 27, 2016; DOI: https://doi.org/10.1007/s12275-016-6157-x

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Panton-Valentine leukocidin-negative methicillin-resistant Staphylococcus aureus (MRSA) clone ST72, known as a major community-associated MRSA in Korea, has emerged as an important pathogen in hospitals. To understand bacterial properties that underlie transformation of this clone into a nosocomial pathogen, we compared characteristics of the community-genotype ST72 MRSA isolates with those of ST5 and ST239 MRSA, which have been predominant nosocomial MRSA clones in Korea. Several genes associated with adhesion and virulence were absent or rarely found in ST72 isolates. Many ST72 isolates (70.1%) belonged to agr group I, but the agr group of other ST72 isolates could not be determined. As indicated by δ-hemolysin production, ST72 isolates expressed fully functional agr, whereas agr dysfunction was observed in ST5 and ST239 isolates. In the biofilm formation assay, no upregulation of biofilm-forming activity of ST72 MRSA was detected. However, ST72 isolates demonstrated persistence under hypotonic and desiccating conditions (survival rates 72.3% and 33.9%, respectively), which was similar to characteristics of ST5 or ST239 isolates. ST72- MRSA isolates showed low virulence, but properties of their functional agr system could facilitate their spread in hospitals. In conclusion, tolerance to stressful environments, e.g., hypotonic and dry conditions, may also contribute to survival of the community-associated MRSA clones in healthcare facilities.

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Research Support, Non-U.S. Gov't

Effect of carbonyl cyanide 3-chlorophenylhydrazone (CCCP) on killing Acinetobacter baumannii by colistin: Young Kyoung Park , Kwan Soo Ko; J. Microbiol. 2015;53(1):53-59. Published online January 4, 2015; DOI: https://doi.org/10.1007/s12275-015-4498-5

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We investigated the effect of cyanide 3-chlorophenylhydrazone (CCCP) and other efflux pump inhibitors (EPIs) on the colistin susceptibility in Acinetobacter baumannii. While minimum inhibitory concentrations (MICs) of colistin in all colistin-resistant strains decreased significantly with 25 μM of CCCP and 2,4-dinitrophenol (DNP), phenyl-arginine-β- naphthylamide (PAβN), and reserpine did not decrease the colistin MICs. However, CCCP and DNP as well as PAβN and reserpine did not have a significant effect on the MICs of the other agents. Efflux pump gene expressions in colistinresistant strains were not increased compared with those in colistin-susceptible strains. When only 5X MIC of colistin (5 mg/L) was provided to a colistin-susceptible A. baumannii strain, the bacterial cell number was reduced by 9 h after exposure to colistin, but regrowth was observed. When CCCP was added to colistin, bacterial cells were completely killed after 24 to 48 h of incubation, which was not due to the toxicity of CCCP itself. Colistin resistance in A. baumannii may not be due to efflux pumps. Our present study suggests that bacterial cells with reduced metabolic activity by CCCP are more susceptible to colistin in A. baumannii. It may show the possibility that combined therapy with colistin and other antimicrobial agents could effective against A. baumannii infections.

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Retraction

Retraction Note to: Cryptic prophages in a blaNDM‑1‑bearing plasmid increase bacterial survival against high NaCl concentration, high and low temperatures, and oxidative and immunological stressors: So Yeon Kim , Kwan Soo Ko; J. Microbiol. 2023;61(4):481-481.; DOI: https://doi.org/10.1007/s12275-023-00049-1

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Abstract PDF: Retraction Note to: Journal of Microbiology (2020) Vol. 58, No. 6, pp. 483–488 https://doi.org/10.1007/s12275-020-9605-6 The Editor-in-Chief has retracted this article at the request of the authors. After publication concerns were raised that prophage sequences do not exist in the genome of the plasmid pNDM-A1 used in this study. The authors have not been able to confirm the existence of prophage sequences in the plasmid. As a result, the Editor-in-Chief no longer has confidence in the results and conclusions presented in this article. Kwan Soo Ko agrees with this retraction. So Yeon Kim has not responded to correspondence from the Editor-in-Chief about this retraction.

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