Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelis
ABSTRACT Elizabethkingia anophelis, a nonfermenting Gram-negative bacterium, causes life-threatening health care-associated infections. E. anophelis harbors multidrug resistance (MDR) genes and is intrinsically resistant to various classes of antibiotics. Outer membrane vesicles (OMVs) are secreted...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-08-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00262-22 |
| _version_ | 1811188251021541376 |
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| author | Ming-Hsien Chiang Fang-Ju Chang Dinesh Kumar Kesavan Aparna Vasudevan Huaxi Xu Kuo-Lun Lan Shu-Wei Huang Hung-Sheng Shang Yi-Ping Chuang Ya-Sung Yang Te-Li Chen |
| author_facet | Ming-Hsien Chiang Fang-Ju Chang Dinesh Kumar Kesavan Aparna Vasudevan Huaxi Xu Kuo-Lun Lan Shu-Wei Huang Hung-Sheng Shang Yi-Ping Chuang Ya-Sung Yang Te-Li Chen |
| author_sort | Ming-Hsien Chiang |
| collection | DOAJ |
| description | ABSTRACT Elizabethkingia anophelis, a nonfermenting Gram-negative bacterium, causes life-threatening health care-associated infections. E. anophelis harbors multidrug resistance (MDR) genes and is intrinsically resistant to various classes of antibiotics. Outer membrane vesicles (OMVs) are secreted by Gram-negative bacteria and contain materials involved in bacterial survival and pathogenesis. OMVs specialize and tailor their functions by carrying different components to challenging environments and allowing communication with other microorganisms or hosts. In this study, we sought to understand the characteristics of E. anophelis OMVs under different antibiotic stress conditions. An extensively drug-resistant clinical isolate, E. anophelis C08, was exposed to multiple antibiotics in vitro, and its OMVs were characterized using nanoparticle tracking analysis, transmission electron microscopy, and proteomic analysis. Protein functionality analysis showed that the OMVs were predominantly involved in metabolism, survival, defense, and antibiotic resistance processes, such as the Rag/Sus family, the chaperonin GroEL, prenyltransferase, and an HmuY family protein. Additionally, a protein-protein interaction network demonstrated that OMVs from imipenem-treated E. anophelis showed significant enrichments in the outer membrane, adenyl nucleotide binding, serine-type peptidase activity, the glycosyl compound metabolic process, and cation binding proteins. Collectively, the OMV proteome expression profile indicates that the role of OMVs is immunologically relevant and related to bacterial survival in antibiotic stress environments rather than representing a resistance point. IMPORTANCE Elizabethkingia anophelis is a bacterium often associated with nosocomial infection. This study demonstrated that imipenem-induced E. anophelis outer membrane vesicles (OMVs) are immunologically relevant and crucial for bacterial survival under antibiotic stress conditions rather than being a source of antibiotic resistance. Furthermore, this is the first study to discuss the protein-protein interaction network of the OMVs released by E. anophelis, especially under antibiotic stress. Our findings provide important insights into clinical antibiotic stewardship. |
| first_indexed | 2024-04-11T14:17:29Z |
| format | Article |
| id | doaj.art-129bbfb9362b46659f04e62c8564bca7 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-11T14:17:29Z |
| publishDate | 2022-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-129bbfb9362b46659f04e62c8564bca72022-12-22T04:19:14ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-08-0110410.1128/spectrum.00262-22Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelisMing-Hsien Chiang0Fang-Ju Chang1Dinesh Kumar Kesavan2Aparna Vasudevan3Huaxi Xu4Kuo-Lun Lan5Shu-Wei Huang6Hung-Sheng Shang7Yi-Ping Chuang8Ya-Sung Yang9Te-Li Chen10Department of Biology and Anatomy, National Defense Medical Center, Taipei, TaiwanDepartment of Biology and Anatomy, National Defense Medical Center, Taipei, TaiwanSchool of Materials Science and Engineering, Nanyang Technological University, Singapore, SingaporeInternational Genomics Research Centre (IGRC), Jiangsu University, Zhenjiang, ChinaInternational Genomics Research Centre (IGRC), Jiangsu University, Zhenjiang, ChinaDivision of Clinical Pathology, Department of Pathology, Tri-Service General Hospital, National Defense Medical Center, Taipei, TaiwanDepartment of Orthopedic Surgery, Wan Fang Hospital, Taipei Medical University, Taipei, TaiwanDivision of Clinical Pathology, Department of Pathology, Tri-Service General Hospital, National Defense Medical Center, Taipei, TaiwanDepartment of Microbiology and Immunology, National Defense Medical Center, Taipei, TaiwanDivision of Infectious Diseases and Tropical Medicine, Department of Internal Medicine, Tri-Service General Hospital, National Defense Medical Center, Taipei, TaiwanGraduate Institute of Life Sciences, National Defense Medical Center, Taipei, TaiwanABSTRACT Elizabethkingia anophelis, a nonfermenting Gram-negative bacterium, causes life-threatening health care-associated infections. E. anophelis harbors multidrug resistance (MDR) genes and is intrinsically resistant to various classes of antibiotics. Outer membrane vesicles (OMVs) are secreted by Gram-negative bacteria and contain materials involved in bacterial survival and pathogenesis. OMVs specialize and tailor their functions by carrying different components to challenging environments and allowing communication with other microorganisms or hosts. In this study, we sought to understand the characteristics of E. anophelis OMVs under different antibiotic stress conditions. An extensively drug-resistant clinical isolate, E. anophelis C08, was exposed to multiple antibiotics in vitro, and its OMVs were characterized using nanoparticle tracking analysis, transmission electron microscopy, and proteomic analysis. Protein functionality analysis showed that the OMVs were predominantly involved in metabolism, survival, defense, and antibiotic resistance processes, such as the Rag/Sus family, the chaperonin GroEL, prenyltransferase, and an HmuY family protein. Additionally, a protein-protein interaction network demonstrated that OMVs from imipenem-treated E. anophelis showed significant enrichments in the outer membrane, adenyl nucleotide binding, serine-type peptidase activity, the glycosyl compound metabolic process, and cation binding proteins. Collectively, the OMV proteome expression profile indicates that the role of OMVs is immunologically relevant and related to bacterial survival in antibiotic stress environments rather than representing a resistance point. IMPORTANCE Elizabethkingia anophelis is a bacterium often associated with nosocomial infection. This study demonstrated that imipenem-induced E. anophelis outer membrane vesicles (OMVs) are immunologically relevant and crucial for bacterial survival under antibiotic stress conditions rather than being a source of antibiotic resistance. Furthermore, this is the first study to discuss the protein-protein interaction network of the OMVs released by E. anophelis, especially under antibiotic stress. Our findings provide important insights into clinical antibiotic stewardship.https://journals.asm.org/doi/10.1128/spectrum.00262-22Elizabethkingia anophelisantibiotic resistanceouter membrane vesicleproteomicsprotein-protein interactions |
| spellingShingle | Ming-Hsien Chiang Fang-Ju Chang Dinesh Kumar Kesavan Aparna Vasudevan Huaxi Xu Kuo-Lun Lan Shu-Wei Huang Hung-Sheng Shang Yi-Ping Chuang Ya-Sung Yang Te-Li Chen Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelis Microbiology Spectrum Elizabethkingia anophelis antibiotic resistance outer membrane vesicle proteomics protein-protein interactions |
| title | Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelis |
| title_full | Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelis |
| title_fullStr | Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelis |
| title_full_unstemmed | Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelis |
| title_short | Proteomic Network of Antibiotic-Induced Outer Membrane Vesicles Released by Extensively Drug-Resistant Elizabethkingia anophelis |
| title_sort | proteomic network of antibiotic induced outer membrane vesicles released by extensively drug resistant elizabethkingia anophelis |
| topic | Elizabethkingia anophelis antibiotic resistance outer membrane vesicle proteomics protein-protein interactions |
| url | https://journals.asm.org/doi/10.1128/spectrum.00262-22 |
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