The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two Mechanisms

Members of the <i>Sphingomonadales</i> are renowned for their ability to degrade polycyclic aromatic hydrocarbons (PAHs). However, little is known about the regulatory mechanisms of the degradative pathway. Using cross-feeding bioassay, a functional LuxI/LuxR-type acyl-homoserine lactone...

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Main Authors: Zhiliang Yu, Zeyu Hu, Qimiao Xu, Mengting Zhang, Nate Yuan, Jiongru Liu, Qiu Meng, Jianhua Yin
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/15/5548
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spelling doaj-61948c5e8e6144449e34256cf3c6bc1a2020-11-25T03:48:35ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-08-01215548554810.3390/ijms21155548The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two MechanismsZhiliang Yu0Zeyu Hu1Qimiao Xu2Mengting Zhang3Nate Yuan4Jiongru Liu5Qiu Meng6Jianhua Yin7College of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaCollege of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaCollege of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaCollege of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaCollege of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaCollege of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaCollege of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaCollege of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou 310014, ChinaMembers of the <i>Sphingomonadales</i> are renowned for their ability to degrade polycyclic aromatic hydrocarbons (PAHs). However, little is known about the regulatory mechanisms of the degradative pathway. Using cross-feeding bioassay, a functional LuxI/LuxR-type acyl-homoserine lactone (AHL)-mediated quorum sensing (QS) system was identified from <i>Croceicoccus naphthovorans</i> PQ-2, a member of the order <i>Sphingomonadales</i>. Inactivation of the QS system resulted in a significant decrease in PAHs degradation. The QS system positively controlled the expression of three PAH-degrading genes (<i>ahdA1e</i>, <i>xylE</i> and <i>xylG</i>) and a regulatory gene <i>ardR</i>, which are located on the large plasmid. Interestingly, the transcription levels of these three PAH-degrading genes were significantly down-regulated in the <i>ardR</i> mutant. In addition, bacterial cell surface hydrophobicity and cell morphology were altered in the QS-deficient mutant. Therefore, the QS system in strain PQ-2 positively regulates PAH degradation via two mechanisms: (i) by induction of PAH-degrading genes directly and/or indirectly; and (ii) by an increase of bacterial cell surface hydrophobicity. The findings of this study improve our understanding of how the QS system influences the degradation of PAHs, therefore facilitating the development of new strategies for the bioremediation of PAHs.https://www.mdpi.com/1422-0067/21/15/5548quorum sensingpolycyclic aromatic hydrocarbonsbiodegradationcell surface hydrophobicity<i>Sphingomonadales</i>
collection DOAJ
language English
format Article
sources DOAJ
author Zhiliang Yu
Zeyu Hu
Qimiao Xu
Mengting Zhang
Nate Yuan
Jiongru Liu
Qiu Meng
Jianhua Yin
spellingShingle Zhiliang Yu
Zeyu Hu
Qimiao Xu
Mengting Zhang
Nate Yuan
Jiongru Liu
Qiu Meng
Jianhua Yin
The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two Mechanisms
International Journal of Molecular Sciences
quorum sensing
polycyclic aromatic hydrocarbons
biodegradation
cell surface hydrophobicity
<i>Sphingomonadales</i>
author_facet Zhiliang Yu
Zeyu Hu
Qimiao Xu
Mengting Zhang
Nate Yuan
Jiongru Liu
Qiu Meng
Jianhua Yin
author_sort Zhiliang Yu
title The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two Mechanisms
title_short The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two Mechanisms
title_full The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two Mechanisms
title_fullStr The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two Mechanisms
title_full_unstemmed The LuxI/LuxR-Type Quorum Sensing System Regulates Degradation of Polycyclic Aromatic Hydrocarbons via Two Mechanisms
title_sort luxi/luxr-type quorum sensing system regulates degradation of polycyclic aromatic hydrocarbons via two mechanisms
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2020-08-01
description Members of the <i>Sphingomonadales</i> are renowned for their ability to degrade polycyclic aromatic hydrocarbons (PAHs). However, little is known about the regulatory mechanisms of the degradative pathway. Using cross-feeding bioassay, a functional LuxI/LuxR-type acyl-homoserine lactone (AHL)-mediated quorum sensing (QS) system was identified from <i>Croceicoccus naphthovorans</i> PQ-2, a member of the order <i>Sphingomonadales</i>. Inactivation of the QS system resulted in a significant decrease in PAHs degradation. The QS system positively controlled the expression of three PAH-degrading genes (<i>ahdA1e</i>, <i>xylE</i> and <i>xylG</i>) and a regulatory gene <i>ardR</i>, which are located on the large plasmid. Interestingly, the transcription levels of these three PAH-degrading genes were significantly down-regulated in the <i>ardR</i> mutant. In addition, bacterial cell surface hydrophobicity and cell morphology were altered in the QS-deficient mutant. Therefore, the QS system in strain PQ-2 positively regulates PAH degradation via two mechanisms: (i) by induction of PAH-degrading genes directly and/or indirectly; and (ii) by an increase of bacterial cell surface hydrophobicity. The findings of this study improve our understanding of how the QS system influences the degradation of PAHs, therefore facilitating the development of new strategies for the bioremediation of PAHs.
topic quorum sensing
polycyclic aromatic hydrocarbons
biodegradation
cell surface hydrophobicity
<i>Sphingomonadales</i>
url https://www.mdpi.com/1422-0067/21/15/5548
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