Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella Pneumoniae
ABSTRACT The coinfection process producing multiple species of pathogens provides a specific ecological niche for the exchange of genetic materials between pathogens, in which plasmids play a vital role in horizontal gene transfer, especially for drug resistance, but the underlying transfer pathway...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.03554-22 |
| _version_ | 1797803373648412672 |
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| author | Jingjing Quan Huangdu Hu Huichuan Zhang Yan Meng Weichao Liao Junxin Zhou Xinhong Han Qiucheng Shi Dongdong Zhao Qian Wang Yan Jiang Yunsong Yu |
| author_facet | Jingjing Quan Huangdu Hu Huichuan Zhang Yan Meng Weichao Liao Junxin Zhou Xinhong Han Qiucheng Shi Dongdong Zhao Qian Wang Yan Jiang Yunsong Yu |
| author_sort | Jingjing Quan |
| collection | DOAJ |
| description | ABSTRACT The coinfection process producing multiple species of pathogens provides a specific ecological niche for the exchange of genetic materials between pathogens, in which plasmids play a vital role in horizontal gene transfer, especially for drug resistance, but the underlying transfer pathway remains unclear. Interspecies communication of the plasmids associated with the transfer of third-generation cephalosporins, quinolones, and colistin resistance has been observed in simultaneously isolated Escherichia coli and Klebsiella pneumoniae from abdominal drainage following surgery. The MICs of antimicrobial agents were determined by the broth microdilution method. The complete chromosome and plasmid sequences were obtained by combining Illumina paired-end short reads and MinION long reads. S1-PFGE, southern blot analysis and conjugation assay confirmed the transferability of the mcr-1-harboring plasmid. Both the E. coli isolate EC15255 and K. pneumoniae isolate KP15255 from the same specimen presented multidrug resistance. Each of them harbored one chromosome and three plasmids, and two plasmids and their mediated resistance could be transferred to the recipient by conjugation. Comparison of their genome sequences suggested that several genetic communication events occurred between species, especially among their plasmids, such as whole-plasmid transfer, insertion, deletion, amplification, or inversion. Exchange of plasmids or the genetic elements they harbor plays a critical role in antimicrobial resistance gene transmission and poses a substantial threat to nosocomial infection control, necessitating the continued surveillance of multidrug resistant pathogens, especially during coinfection. IMPORTANCE The genome sequence of bacterial pathogens commonly provides a detailed clue of genetic communication among clones or even distinct species. The intestinal microecological environment is a representative ecological niche for genetic communication. However, it is still difficult to describe the details of horizontal gene transfer or other genetic events within them because the evidence in the genome sequence is incomplete and limited. In this study, the simultaneously isolated Escherichia coli and Klebsiella pneumoniae from a coinfection process provided an excellent example for observation of interspecies communication between the two genomes and the plasmids they harbor. A complete genome sequence acquired by combining the Illumina and MinION sequencing platforms facilitated the understanding of genetic communication events, such as whole-plasmid transfer, insertion, deletion, amplification, or inversion, which contribute to antimicrobial resistance gene transmission and are a substantial threat to nosocomial infection control. |
| first_indexed | 2024-03-13T05:20:54Z |
| format | Article |
| id | doaj.art-134e4fe1c34c4e8a9a5775af5c40e2be |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:20:54Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-134e4fe1c34c4e8a9a5775af5c40e2be2023-06-15T13:18:32ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.03554-22Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella PneumoniaeJingjing Quan0Huangdu Hu1Huichuan Zhang2Yan Meng3Weichao Liao4Junxin Zhou5Xinhong Han6Qiucheng Shi7Dongdong Zhao8Qian Wang9Yan Jiang10Yunsong Yu11Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Clinical Laboratory, Zhejiang Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Intensive Care Unit, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of General Practice, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaABSTRACT The coinfection process producing multiple species of pathogens provides a specific ecological niche for the exchange of genetic materials between pathogens, in which plasmids play a vital role in horizontal gene transfer, especially for drug resistance, but the underlying transfer pathway remains unclear. Interspecies communication of the plasmids associated with the transfer of third-generation cephalosporins, quinolones, and colistin resistance has been observed in simultaneously isolated Escherichia coli and Klebsiella pneumoniae from abdominal drainage following surgery. The MICs of antimicrobial agents were determined by the broth microdilution method. The complete chromosome and plasmid sequences were obtained by combining Illumina paired-end short reads and MinION long reads. S1-PFGE, southern blot analysis and conjugation assay confirmed the transferability of the mcr-1-harboring plasmid. Both the E. coli isolate EC15255 and K. pneumoniae isolate KP15255 from the same specimen presented multidrug resistance. Each of them harbored one chromosome and three plasmids, and two plasmids and their mediated resistance could be transferred to the recipient by conjugation. Comparison of their genome sequences suggested that several genetic communication events occurred between species, especially among their plasmids, such as whole-plasmid transfer, insertion, deletion, amplification, or inversion. Exchange of plasmids or the genetic elements they harbor plays a critical role in antimicrobial resistance gene transmission and poses a substantial threat to nosocomial infection control, necessitating the continued surveillance of multidrug resistant pathogens, especially during coinfection. IMPORTANCE The genome sequence of bacterial pathogens commonly provides a detailed clue of genetic communication among clones or even distinct species. The intestinal microecological environment is a representative ecological niche for genetic communication. However, it is still difficult to describe the details of horizontal gene transfer or other genetic events within them because the evidence in the genome sequence is incomplete and limited. In this study, the simultaneously isolated Escherichia coli and Klebsiella pneumoniae from a coinfection process provided an excellent example for observation of interspecies communication between the two genomes and the plasmids they harbor. A complete genome sequence acquired by combining the Illumina and MinION sequencing platforms facilitated the understanding of genetic communication events, such as whole-plasmid transfer, insertion, deletion, amplification, or inversion, which contribute to antimicrobial resistance gene transmission and are a substantial threat to nosocomial infection control.https://journals.asm.org/doi/10.1128/spectrum.03554-22interspeciesplasmidcolistinmcr-1IS26 |
| spellingShingle | Jingjing Quan Huangdu Hu Huichuan Zhang Yan Meng Weichao Liao Junxin Zhou Xinhong Han Qiucheng Shi Dongdong Zhao Qian Wang Yan Jiang Yunsong Yu Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella Pneumoniae Microbiology Spectrum interspecies plasmid colistin mcr-1 IS26 |
| title | Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella Pneumoniae |
| title_full | Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella Pneumoniae |
| title_fullStr | Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella Pneumoniae |
| title_full_unstemmed | Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella Pneumoniae |
| title_short | Investigating Possible Interspecies Communication of Plasmids Associated with Transfer of Third-Generation Cephalosporin, Quinolone, and Colistin Resistance Between Simultaneously Isolated Escherichia Coli and Klebsiella Pneumoniae |
| title_sort | investigating possible interspecies communication of plasmids associated with transfer of third generation cephalosporin quinolone and colistin resistance between simultaneously isolated escherichia coli and klebsiella pneumoniae |
| topic | interspecies plasmid colistin mcr-1 IS26 |
| url | https://journals.asm.org/doi/10.1128/spectrum.03554-22 |
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