Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosa

With the prevalence of multidrug-resistant bacteria and clinical -acquired pathogenic infections, the development of quorum-sensing (QS) interfering agents is one of the most potential strategies to combat bacterial infections and antibiotic resistance. Chinese herbal medicines constitute a valuable...

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Main Authors: Dan Yang, Suqi Hao, Ling Zhao, Fei Shi, Gang Ye, Yuanfeng Zou, Xu Song, Lixia Li, Zhongqiong Yin, Xiaoli He, Shiling Feng, Helin Chen, Yu Zhang, Yuanze Gao, Yinglun Li, Huaqiao Tang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.692474/full
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author Dan Yang
Suqi Hao
Ling Zhao
Fei Shi
Gang Ye
Yuanfeng Zou
Xu Song
Lixia Li
Zhongqiong Yin
Xiaoli He
Shiling Feng
Helin Chen
Yu Zhang
Yuanze Gao
Yinglun Li
Huaqiao Tang
author_facet Dan Yang
Suqi Hao
Ling Zhao
Fei Shi
Gang Ye
Yuanfeng Zou
Xu Song
Lixia Li
Zhongqiong Yin
Xiaoli He
Shiling Feng
Helin Chen
Yu Zhang
Yuanze Gao
Yinglun Li
Huaqiao Tang
author_sort Dan Yang
collection DOAJ
description With the prevalence of multidrug-resistant bacteria and clinical -acquired pathogenic infections, the development of quorum-sensing (QS) interfering agents is one of the most potential strategies to combat bacterial infections and antibiotic resistance. Chinese herbal medicines constitute a valuable bank of resources for the identification of QS inhibitors. Accordingly, in this research, some compounds were tested for QS inhibition using indicator strains. Paeonol is a phenolic compound, which can effectively reduce the production of violacein without affecting its growth in Chromobacterium violaceum ATCC 12472, indicating its excellent anti-QS activity. This study assessed the anti-biofilm activity of paeonol against Gram-negative pathogens and investigated the effect of paeonol on QS-regulated virulence factors in Pseudomonas aeruginosa. A Caenorhabditis elegans infection model was used to explore the anti-infection ability of paeonol in vivo. Paeonol exhibited an effective anti-biofilm activity against Gram-negative bacteria. The ability of paeonol to interfere with the AHL-mediated quorum sensing systems of P. aeruginosa was determined, found that it could attenuate biofilm formation, and synthesis of pyocyanin, protease, elastase, motility, and AHL signaling molecule in a concentration- and time-dependent manner. Moreover, paeonol could significantly downregulate the transcription level of the QS-related genes of P. aeruginosa including lasI/R, rhlI/R, pqs/mvfR, as well as mediated its virulence factors, lasA, lasB, rhlA, rhlC, phzA, phzM, phzH, and phzS. In vivo studies revealed that paeonol could reduce the pathogenicity of P. aeruginosa and enhance the survival rate of C. elegans, showing a moderate protective effect on C. elegans. Collectively, these findings suggest that paeonol attenuates bacterial virulence and infection of P. aeruginosa and that further research elucidating the anti-QS mechanism of this compound in vivo is warranted.
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spelling doaj.art-3992f7fbf65444e2aba99ba965ac79582022-12-21T18:31:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-08-011210.3389/fmicb.2021.692474692474Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosaDan Yang0Suqi Hao1Ling Zhao2Fei Shi3Gang Ye4Yuanfeng Zou5Xu Song6Lixia Li7Zhongqiong Yin8Xiaoli He9Shiling Feng10Helin Chen11Yu Zhang12Yuanze Gao13Yinglun Li14Huaqiao Tang15College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Science, Sichuan Agricultural University, Chengdu, ChinaCollege of Life Science, Sichuan Agricultural University, Yaan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, ChinaWith the prevalence of multidrug-resistant bacteria and clinical -acquired pathogenic infections, the development of quorum-sensing (QS) interfering agents is one of the most potential strategies to combat bacterial infections and antibiotic resistance. Chinese herbal medicines constitute a valuable bank of resources for the identification of QS inhibitors. Accordingly, in this research, some compounds were tested for QS inhibition using indicator strains. Paeonol is a phenolic compound, which can effectively reduce the production of violacein without affecting its growth in Chromobacterium violaceum ATCC 12472, indicating its excellent anti-QS activity. This study assessed the anti-biofilm activity of paeonol against Gram-negative pathogens and investigated the effect of paeonol on QS-regulated virulence factors in Pseudomonas aeruginosa. A Caenorhabditis elegans infection model was used to explore the anti-infection ability of paeonol in vivo. Paeonol exhibited an effective anti-biofilm activity against Gram-negative bacteria. The ability of paeonol to interfere with the AHL-mediated quorum sensing systems of P. aeruginosa was determined, found that it could attenuate biofilm formation, and synthesis of pyocyanin, protease, elastase, motility, and AHL signaling molecule in a concentration- and time-dependent manner. Moreover, paeonol could significantly downregulate the transcription level of the QS-related genes of P. aeruginosa including lasI/R, rhlI/R, pqs/mvfR, as well as mediated its virulence factors, lasA, lasB, rhlA, rhlC, phzA, phzM, phzH, and phzS. In vivo studies revealed that paeonol could reduce the pathogenicity of P. aeruginosa and enhance the survival rate of C. elegans, showing a moderate protective effect on C. elegans. Collectively, these findings suggest that paeonol attenuates bacterial virulence and infection of P. aeruginosa and that further research elucidating the anti-QS mechanism of this compound in vivo is warranted.https://www.frontiersin.org/articles/10.3389/fmicb.2021.692474/fullpaeonolquorum sensingPseudomonas aeruginosaanti-virulencebiofilm
spellingShingle Dan Yang
Suqi Hao
Ling Zhao
Fei Shi
Gang Ye
Yuanfeng Zou
Xu Song
Lixia Li
Zhongqiong Yin
Xiaoli He
Shiling Feng
Helin Chen
Yu Zhang
Yuanze Gao
Yinglun Li
Huaqiao Tang
Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosa
Frontiers in Microbiology
paeonol
quorum sensing
Pseudomonas aeruginosa
anti-virulence
biofilm
title Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosa
title_full Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosa
title_fullStr Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosa
title_full_unstemmed Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosa
title_short Paeonol Attenuates Quorum-Sensing Regulated Virulence and Biofilm Formation in Pseudomonas aeruginosa
title_sort paeonol attenuates quorum sensing regulated virulence and biofilm formation in pseudomonas aeruginosa
topic paeonol
quorum sensing
Pseudomonas aeruginosa
anti-virulence
biofilm
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.692474/full
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