Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic condition

Gram-positive Enterococcus faecium exhibited higher susceptibility (>4-fold) to polymyxin B (PMB), the canonical antimicrobial peptide against Gram-negative bacteria, under anaerobic condition than aerobic condition. Anaerobically grown E. faecium exhibited high vulnerability to PMB, leading to a...

Full description

Saved in:
Bibliographic Details
Main Authors: Yongjun Son, Bitnara Kim, Pureun Kim, Jihyeon Min, Yerim Park, Jihye Yang, Wonjae Kim, Masanori Toyofuku, Woojun Park
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2024.2438465
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850124340567212032
author Yongjun Son
Bitnara Kim
Pureun Kim
Jihyeon Min
Yerim Park
Jihye Yang
Wonjae Kim
Masanori Toyofuku
Woojun Park
author_facet Yongjun Son
Bitnara Kim
Pureun Kim
Jihyeon Min
Yerim Park
Jihye Yang
Wonjae Kim
Masanori Toyofuku
Woojun Park
author_sort Yongjun Son
collection DOAJ
description Gram-positive Enterococcus faecium exhibited higher susceptibility (>4-fold) to polymyxin B (PMB), the canonical antimicrobial peptide against Gram-negative bacteria, under anaerobic condition than aerobic condition. Anaerobically grown E. faecium exhibited high vulnerability to PMB, leading to alteration of cell surface and morphology, as observed based on their high dansyl-PMB affinity (>2.9-fold), a proportion (>8.5-fold) of propidium iodide-stained cells, and observation of scanning electron microscopy results. Interestingly, our transcriptomic and chemical analyses revealed that enterocin B, produced anaerobically, imposes a burden on the cellular envelope when cells are exposed to PMB. This scenario was also supported by PMB susceptibility tests and killing curves, which showed that ΔentB knockout mutant cells were more resistant to PMB (32 µg/mL) compared to wild-type cells (4 µg/mL) under anaerobic condition. Fluorescent D-amino acid and BOCILLIN™-fluorescent profiling of transpeptidase activities in ΔentB mutant cells under anaerobic condition revealed similar levels of activity to those observed in WT cells under aerobic condition. The high level of secreted bacteriocins in WT under anaerobic condition likely led to significant membrane depolarization and loosening of the peptidoglycan layer, making the cells more permeable to PMB. Overall, our findings suggest that anaerobically produced bacteriocins, in conjunction with PMB, contribute to the killing of E. faecium by destabilizing its cell envelope.
format Article
id doaj-art-3c020c4cad6b4ee2bc8ff0879e68585a
institution OA Journals
issn 1949-0976
1949-0984
language English
publishDate 2024-12-01
publisher Taylor & Francis Group
record_format Article
series Gut Microbes
spelling doaj-art-3c020c4cad6b4ee2bc8ff0879e68585a2025-08-20T02:34:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842024-12-0116110.1080/19490976.2024.2438465Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic conditionYongjun Son0Bitnara Kim1Pureun Kim2Jihyeon Min3Yerim Park4Jihye Yang5Wonjae Kim6Masanori Toyofuku7Woojun Park8Laboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaLaboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaLaboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaLaboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaLaboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaLaboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaLaboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaDepartment of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanLaboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of KoreaGram-positive Enterococcus faecium exhibited higher susceptibility (>4-fold) to polymyxin B (PMB), the canonical antimicrobial peptide against Gram-negative bacteria, under anaerobic condition than aerobic condition. Anaerobically grown E. faecium exhibited high vulnerability to PMB, leading to alteration of cell surface and morphology, as observed based on their high dansyl-PMB affinity (>2.9-fold), a proportion (>8.5-fold) of propidium iodide-stained cells, and observation of scanning electron microscopy results. Interestingly, our transcriptomic and chemical analyses revealed that enterocin B, produced anaerobically, imposes a burden on the cellular envelope when cells are exposed to PMB. This scenario was also supported by PMB susceptibility tests and killing curves, which showed that ΔentB knockout mutant cells were more resistant to PMB (32 µg/mL) compared to wild-type cells (4 µg/mL) under anaerobic condition. Fluorescent D-amino acid and BOCILLIN™-fluorescent profiling of transpeptidase activities in ΔentB mutant cells under anaerobic condition revealed similar levels of activity to those observed in WT cells under aerobic condition. The high level of secreted bacteriocins in WT under anaerobic condition likely led to significant membrane depolarization and loosening of the peptidoglycan layer, making the cells more permeable to PMB. Overall, our findings suggest that anaerobically produced bacteriocins, in conjunction with PMB, contribute to the killing of E. faecium by destabilizing its cell envelope.https://www.tandfonline.com/doi/10.1080/19490976.2024.2438465Enterococcus faeciumpolymyxin Bfacultative anaerobeantibiotic resistancebacteriocinpeptidoglycan
spellingShingle Yongjun Son
Bitnara Kim
Pureun Kim
Jihyeon Min
Yerim Park
Jihye Yang
Wonjae Kim
Masanori Toyofuku
Woojun Park
Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic condition
Gut Microbes
Enterococcus faecium
polymyxin B
facultative anaerobe
antibiotic resistance
bacteriocin
peptidoglycan
title Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic condition
title_full Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic condition
title_fullStr Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic condition
title_full_unstemmed Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic condition
title_short Unexpected vulnerability of Enterococcus faecium to polymyxin B under anaerobic condition
title_sort unexpected vulnerability of enterococcus faecium to polymyxin b under anaerobic condition
topic Enterococcus faecium
polymyxin B
facultative anaerobe
antibiotic resistance
bacteriocin
peptidoglycan
url https://www.tandfonline.com/doi/10.1080/19490976.2024.2438465
work_keys_str_mv AT yongjunson unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT bitnarakim unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT pureunkim unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT jihyeonmin unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT yerimpark unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT jihyeyang unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT wonjaekim unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT masanoritoyofuku unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition
AT woojunpark unexpectedvulnerabilityofenterococcusfaeciumtopolymyxinbunderanaerobiccondition