Cargando…

Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa

BACKGROUND: Pseudomonas aeruginosa (P. aeruginosa) has been majorly implicated in the infection of burns, wounds, skin, and respiratory tract. Colistin is considered the last line of defense against P. aeruginosa infections. However, colistin is becoming increasingly invalid in treating patients inf...

Descripción completa

Detalles Bibliográficos
Autores principales: Feng, Luozhu, Xu, Mengxin, Zeng, Weiliang, Zhang, Xiaodong, Wang, Sipei, Yao, Zhuocheng, Zhou, Tieli, Shi, Shiyi, Cao, Jianming, Chen, Lijiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9762083/
https://www.ncbi.nlm.nih.gov/pubmed/36529724
http://dx.doi.org/10.1186/s12866-022-02716-6
_version_ 1784852797355720704
author Feng, Luozhu
Xu, Mengxin
Zeng, Weiliang
Zhang, Xiaodong
Wang, Sipei
Yao, Zhuocheng
Zhou, Tieli
Shi, Shiyi
Cao, Jianming
Chen, Lijiang
author_facet Feng, Luozhu
Xu, Mengxin
Zeng, Weiliang
Zhang, Xiaodong
Wang, Sipei
Yao, Zhuocheng
Zhou, Tieli
Shi, Shiyi
Cao, Jianming
Chen, Lijiang
author_sort Feng, Luozhu
collection PubMed
description BACKGROUND: Pseudomonas aeruginosa (P. aeruginosa) has been majorly implicated in the infection of burns, wounds, skin, and respiratory tract. Colistin is considered the last line of defense against P. aeruginosa infections. However, colistin is becoming increasingly invalid in treating patients infected with colistin-resistant (COL-R) P. aeruginosa. As one of the disinfectants used for wound infections, acetic acid (AA) offers good antibacterial and antibiofilm activities against P. aeruginosa. This study investigated the effects of AA on COL-R P. aeruginosa in terms of its antibacterial, antibiofilm, and anti-virulence properties and the corresponding underlying mechanisms. RESULTS: The antimicrobial susceptibility and growth curve data revealed that 0.078% (v/v) AA exhibited good antibacterial activity against COL-R P. aeruginosa. Subinhibitory concentrations of AA were ineffective in inhibiting biofilm formation, but 4 × and 8 × of the minimum inhibitory concentration (MIC) was effective in removing the preformed biofilms in biofilm-eradication assays. The virulence results illustrated that AA inhibited COL-R P. aeruginosa swimming, swarming, twitching, and pyocyanin and elastase production. The analysis of the potential antibacterial mechanisms of AA on COL-R P. aeruginosa revealed that AA acted by increasing the outer and inner membrane permeability, polarizing the membrane potential, and decreasing the reduction potential in a concentration-dependent manner. The qRT-PCR results revealed that AA may inhibit the virulence of COL-R P. aeruginosa by inhibiting the expression of T3SS-related and QS-related genes. CONCLUSIONS: AA possesses antibacterial, antibiofilm, and anti-virulence properties that ultimately lead to the alteration of the bacterial membrane permeability, membrane potential, and reduction potential. Our findings indicated that AA is presently one of the effective treatment options for infections. A high concentration of AA (> 0.156% v/v) can be used to sterilize biofilm-prone surgical instruments, for hospital disinfection, and for treating the external wound, whereas a low concentration of AA (0.00975–0.039% v/v) may be used as an anti-virulence agent for adjuvant treatment of COL-R P. aeruginosa, thereby further improving the application value of AA in the treatment of infections. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-022-02716-6.
format Online
Article
Text
id pubmed-9762083
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-97620832022-12-20 Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa Feng, Luozhu Xu, Mengxin Zeng, Weiliang Zhang, Xiaodong Wang, Sipei Yao, Zhuocheng Zhou, Tieli Shi, Shiyi Cao, Jianming Chen, Lijiang BMC Microbiol Research BACKGROUND: Pseudomonas aeruginosa (P. aeruginosa) has been majorly implicated in the infection of burns, wounds, skin, and respiratory tract. Colistin is considered the last line of defense against P. aeruginosa infections. However, colistin is becoming increasingly invalid in treating patients infected with colistin-resistant (COL-R) P. aeruginosa. As one of the disinfectants used for wound infections, acetic acid (AA) offers good antibacterial and antibiofilm activities against P. aeruginosa. This study investigated the effects of AA on COL-R P. aeruginosa in terms of its antibacterial, antibiofilm, and anti-virulence properties and the corresponding underlying mechanisms. RESULTS: The antimicrobial susceptibility and growth curve data revealed that 0.078% (v/v) AA exhibited good antibacterial activity against COL-R P. aeruginosa. Subinhibitory concentrations of AA were ineffective in inhibiting biofilm formation, but 4 × and 8 × of the minimum inhibitory concentration (MIC) was effective in removing the preformed biofilms in biofilm-eradication assays. The virulence results illustrated that AA inhibited COL-R P. aeruginosa swimming, swarming, twitching, and pyocyanin and elastase production. The analysis of the potential antibacterial mechanisms of AA on COL-R P. aeruginosa revealed that AA acted by increasing the outer and inner membrane permeability, polarizing the membrane potential, and decreasing the reduction potential in a concentration-dependent manner. The qRT-PCR results revealed that AA may inhibit the virulence of COL-R P. aeruginosa by inhibiting the expression of T3SS-related and QS-related genes. CONCLUSIONS: AA possesses antibacterial, antibiofilm, and anti-virulence properties that ultimately lead to the alteration of the bacterial membrane permeability, membrane potential, and reduction potential. Our findings indicated that AA is presently one of the effective treatment options for infections. A high concentration of AA (> 0.156% v/v) can be used to sterilize biofilm-prone surgical instruments, for hospital disinfection, and for treating the external wound, whereas a low concentration of AA (0.00975–0.039% v/v) may be used as an anti-virulence agent for adjuvant treatment of COL-R P. aeruginosa, thereby further improving the application value of AA in the treatment of infections. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-022-02716-6. BioMed Central 2022-12-19 /pmc/articles/PMC9762083/ /pubmed/36529724 http://dx.doi.org/10.1186/s12866-022-02716-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Feng, Luozhu
Xu, Mengxin
Zeng, Weiliang
Zhang, Xiaodong
Wang, Sipei
Yao, Zhuocheng
Zhou, Tieli
Shi, Shiyi
Cao, Jianming
Chen, Lijiang
Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa
title Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa
title_full Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa
title_fullStr Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa
title_full_unstemmed Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa
title_short Evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant Pseudomonas aeruginosa
title_sort evaluation of the antibacterial, antibiofilm, and anti-virulence effects of acetic acid and the related mechanisms on colistin-resistant pseudomonas aeruginosa
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9762083/
https://www.ncbi.nlm.nih.gov/pubmed/36529724
http://dx.doi.org/10.1186/s12866-022-02716-6
work_keys_str_mv AT fengluozhu evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT xumengxin evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT zengweiliang evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT zhangxiaodong evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT wangsipei evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT yaozhuocheng evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT zhoutieli evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT shishiyi evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT caojianming evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa
AT chenlijiang evaluationoftheantibacterialantibiofilmandantivirulenceeffectsofaceticacidandtherelatedmechanismsoncolistinresistantpseudomonasaeruginosa