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Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities

N-Acyl homoserine lactones (AHLs) are signaling molecules used in the quorum sensing (QS) of Gram-negative bacteria. Some bacteria interfere with the QS system using AHL-inactivating enzymes, commonly known as quorum-quenching (QQ) enzymes. We have recently isolated a new QQ bacterium showing high r...

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Autores principales: Kusada, Hiroyuki, Zhang, Yu, Tamaki, Hideyuki, Kimura, Nobutada, Kamagata, Yoichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6426785/
https://www.ncbi.nlm.nih.gov/pubmed/30923518
http://dx.doi.org/10.3389/fmicb.2019.00455
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author Kusada, Hiroyuki
Zhang, Yu
Tamaki, Hideyuki
Kimura, Nobutada
Kamagata, Yoichi
author_facet Kusada, Hiroyuki
Zhang, Yu
Tamaki, Hideyuki
Kimura, Nobutada
Kamagata, Yoichi
author_sort Kusada, Hiroyuki
collection PubMed
description N-Acyl homoserine lactones (AHLs) are signaling molecules used in the quorum sensing (QS) of Gram-negative bacteria. Some bacteria interfere with the QS system using AHL-inactivating enzymes, commonly known as quorum-quenching (QQ) enzymes. We have recently isolated a new QQ bacterium showing high resistance to multiple β-lactam antibiotics, and its QQ enzyme (MacQ) confers β-lactam antibiotic resistance and exhibits QQ activities. This observation suggests the possibility of isolating novel QQ bacteria from β-lactam antibiotic-resistant bacteria. In this direction, we attempted to isolate penicillin G (PENG)-resistant bacteria from penicillin-contaminated river sediments and activated sludge treating penicillin-containing wastewater and characterize their QQ activities. Of 19 PENG-resistant isolates, six isolates showed high QQ activity toward a broad range of AHLs, including AHLs with 3-oxo substituents. Five of the six AHL-degraders showed AHL-acylase activity and hydrolyzed the amide bond of AHLs, whereas the remaining one strain did not show AHL-acylase activity, suggesting that this isolate may likely possess alternative degradation mechanism such as AHL-lactonase activity hydrolyzing the lactone ring of AHLs. The 16S rRNA gene sequence analysis results categorized these six AHL-degrading isolates into at least five genera, namely, Sphingomonas (Alphaproteobacteria), Diaphorobacter (Betaproteobacteria), Acidovorax (Betaproteobacteria), Stenotrophomonas (Gammaproteobacteria), and Mycobacterium (Actinobacteria); of these, Mycobacterium sp. M1 has never been known as QQ bacteria. Moreover, multiple β-lactam antibiotics showed high minimum inhibitory concentrations (MICs) when tested against all of isolates. These results strongly demonstrate that a wide variety of β-lactam antibiotic-resistant bacteria possess QQ activities. Although the genetic and enzymatic elements are yet unclear, this study may infer the functional and evolutionary correlation between β-lactam antibiotic resistance and QQ activities.
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spelling pubmed-64267852019-03-28 Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities Kusada, Hiroyuki Zhang, Yu Tamaki, Hideyuki Kimura, Nobutada Kamagata, Yoichi Front Microbiol Microbiology N-Acyl homoserine lactones (AHLs) are signaling molecules used in the quorum sensing (QS) of Gram-negative bacteria. Some bacteria interfere with the QS system using AHL-inactivating enzymes, commonly known as quorum-quenching (QQ) enzymes. We have recently isolated a new QQ bacterium showing high resistance to multiple β-lactam antibiotics, and its QQ enzyme (MacQ) confers β-lactam antibiotic resistance and exhibits QQ activities. This observation suggests the possibility of isolating novel QQ bacteria from β-lactam antibiotic-resistant bacteria. In this direction, we attempted to isolate penicillin G (PENG)-resistant bacteria from penicillin-contaminated river sediments and activated sludge treating penicillin-containing wastewater and characterize their QQ activities. Of 19 PENG-resistant isolates, six isolates showed high QQ activity toward a broad range of AHLs, including AHLs with 3-oxo substituents. Five of the six AHL-degraders showed AHL-acylase activity and hydrolyzed the amide bond of AHLs, whereas the remaining one strain did not show AHL-acylase activity, suggesting that this isolate may likely possess alternative degradation mechanism such as AHL-lactonase activity hydrolyzing the lactone ring of AHLs. The 16S rRNA gene sequence analysis results categorized these six AHL-degrading isolates into at least five genera, namely, Sphingomonas (Alphaproteobacteria), Diaphorobacter (Betaproteobacteria), Acidovorax (Betaproteobacteria), Stenotrophomonas (Gammaproteobacteria), and Mycobacterium (Actinobacteria); of these, Mycobacterium sp. M1 has never been known as QQ bacteria. Moreover, multiple β-lactam antibiotics showed high minimum inhibitory concentrations (MICs) when tested against all of isolates. These results strongly demonstrate that a wide variety of β-lactam antibiotic-resistant bacteria possess QQ activities. Although the genetic and enzymatic elements are yet unclear, this study may infer the functional and evolutionary correlation between β-lactam antibiotic resistance and QQ activities. Frontiers Media S.A. 2019-03-14 /pmc/articles/PMC6426785/ /pubmed/30923518 http://dx.doi.org/10.3389/fmicb.2019.00455 Text en Copyright © 2019 Kusada, Zhang, Tamaki, Kimura and Kamagata. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Kusada, Hiroyuki
Zhang, Yu
Tamaki, Hideyuki
Kimura, Nobutada
Kamagata, Yoichi
Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities
title Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities
title_full Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities
title_fullStr Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities
title_full_unstemmed Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities
title_short Novel N-Acyl Homoserine Lactone-Degrading Bacteria Isolated From Penicillin-Contaminated Environments and Their Quorum-Quenching Activities
title_sort novel n-acyl homoserine lactone-degrading bacteria isolated from penicillin-contaminated environments and their quorum-quenching activities
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6426785/
https://www.ncbi.nlm.nih.gov/pubmed/30923518
http://dx.doi.org/10.3389/fmicb.2019.00455
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