2(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscus

Bacterial quorum sensing (QS) is a chemical communication that allows bacteria to coordinate their population and gene regulation in response to threshold concentrations of QS signals. Here, we study the effect of QS inhibitor 2(5H)-furanone (FUR) on the formation of Pseudoalteromonas marina ECSMB14...

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Main Authors: Yi-Feng Li, Xin Zhu, Zhi-Yang Cheng, Xiao Liang, You-Ting Zhu, Dan-Dan Feng, Sergey Dobretsov, Jin-Long Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmars.2020.564075/full
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author Yi-Feng Li
Yi-Feng Li
Yi-Feng Li
Xin Zhu
Xin Zhu
Zhi-Yang Cheng
Zhi-Yang Cheng
Xiao Liang
Xiao Liang
Xiao Liang
You-Ting Zhu
You-Ting Zhu
You-Ting Zhu
Dan-Dan Feng
Dan-Dan Feng
Dan-Dan Feng
Sergey Dobretsov
Sergey Dobretsov
Jin-Long Yang
Jin-Long Yang
Jin-Long Yang
author_facet Yi-Feng Li
Yi-Feng Li
Yi-Feng Li
Xin Zhu
Xin Zhu
Zhi-Yang Cheng
Zhi-Yang Cheng
Xiao Liang
Xiao Liang
Xiao Liang
You-Ting Zhu
You-Ting Zhu
You-Ting Zhu
Dan-Dan Feng
Dan-Dan Feng
Dan-Dan Feng
Sergey Dobretsov
Sergey Dobretsov
Jin-Long Yang
Jin-Long Yang
Jin-Long Yang
author_sort Yi-Feng Li
collection DOAJ
description Bacterial quorum sensing (QS) is a chemical communication that allows bacteria to coordinate their population and gene regulation in response to threshold concentrations of QS signals. Here, we study the effect of QS inhibitor 2(5H)-furanone (FUR) on the formation of Pseudoalteromonas marina ECSMB14103 biofilms and the effect of these biofilms on the settlement of plantigrades of the mussel Mytilus coruscus. FUR was added during biofilm formation of P. marina ECSMB14103 or in the settlement bioassay. FUR at 10–4 M added during biofilm formation significantly (p < 0.05) reduced the settlement of plantigrades, and it was associated with a significant (p < 0.05) reduction of bacterial density. The visualization of individual substances in biofilms shows that β-polysaccharides are the major components in the biofilm matrix. The decreased settlement rate may be attributed to the reduction of the biovolume of α-polysaccharides and β-polysaccharides in biofilms. The transcriptome of biofilms treated with 10–4 M FUR shows 61 genes are differentially expressed. Aspartate kinase and the flagellar assembly protein fliH gene are significantly affected after exposure to 10–4 M FUR (p < 0.05). They are involved in the synthesis of the bacterial cell wall and the mobility of bacteria, respectively. Exposure to 10–4 M FUR also significantly changes the carbapenem biosynthesis pathway, which is regulated by the QS system in bacteria (p < 0.05). These data suggest that FUR directly affects biofilm formation by altering extracellular polymeric substances (EPS) components and metabolic processes, which, in turn, indirectly reduce the settlement of plantigrades. The present study provides new insights into the molecular mechanisms of controlling biofouling.
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spelling doaj.art-7c40b6dfe93147db902c11503be2ed862022-12-22T00:02:37ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452020-09-01710.3389/fmars.2020.5640755640752(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscusYi-Feng Li0Yi-Feng Li1Yi-Feng Li2Xin Zhu3Xin Zhu4Zhi-Yang Cheng5Zhi-Yang Cheng6Xiao Liang7Xiao Liang8Xiao Liang9You-Ting Zhu10You-Ting Zhu11You-Ting Zhu12Dan-Dan Feng13Dan-Dan Feng14Dan-Dan Feng15Sergey Dobretsov16Sergey Dobretsov17Jin-Long Yang18Jin-Long Yang19Jin-Long Yang20International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaSouthern Marine Science and Engineering Guangdong Laboratory, Guangzhou, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaSouthern Marine Science and Engineering Guangdong Laboratory, Guangzhou, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaSouthern Marine Science and Engineering Guangdong Laboratory, Guangzhou, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaSouthern Marine Science and Engineering Guangdong Laboratory, Guangzhou, ChinaDepartment of Marine Science and Fisheries, College of Agricultural and Marine Sciences, Sultan Qaboos University, Muscat, OmanCenter of Excellence in Marine Biotechnology, Sultan Qaboos University, Muscat, OmanInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaSouthern Marine Science and Engineering Guangdong Laboratory, Guangzhou, ChinaBacterial quorum sensing (QS) is a chemical communication that allows bacteria to coordinate their population and gene regulation in response to threshold concentrations of QS signals. Here, we study the effect of QS inhibitor 2(5H)-furanone (FUR) on the formation of Pseudoalteromonas marina ECSMB14103 biofilms and the effect of these biofilms on the settlement of plantigrades of the mussel Mytilus coruscus. FUR was added during biofilm formation of P. marina ECSMB14103 or in the settlement bioassay. FUR at 10–4 M added during biofilm formation significantly (p < 0.05) reduced the settlement of plantigrades, and it was associated with a significant (p < 0.05) reduction of bacterial density. The visualization of individual substances in biofilms shows that β-polysaccharides are the major components in the biofilm matrix. The decreased settlement rate may be attributed to the reduction of the biovolume of α-polysaccharides and β-polysaccharides in biofilms. The transcriptome of biofilms treated with 10–4 M FUR shows 61 genes are differentially expressed. Aspartate kinase and the flagellar assembly protein fliH gene are significantly affected after exposure to 10–4 M FUR (p < 0.05). They are involved in the synthesis of the bacterial cell wall and the mobility of bacteria, respectively. Exposure to 10–4 M FUR also significantly changes the carbapenem biosynthesis pathway, which is regulated by the QS system in bacteria (p < 0.05). These data suggest that FUR directly affects biofilm formation by altering extracellular polymeric substances (EPS) components and metabolic processes, which, in turn, indirectly reduce the settlement of plantigrades. The present study provides new insights into the molecular mechanisms of controlling biofouling.https://www.frontiersin.org/article/10.3389/fmars.2020.564075/fullRNA-sequencingfuranonemarine bacterial biofilmbiofilm matrixplantigrade settlementMytilus coruscus
spellingShingle Yi-Feng Li
Yi-Feng Li
Yi-Feng Li
Xin Zhu
Xin Zhu
Zhi-Yang Cheng
Zhi-Yang Cheng
Xiao Liang
Xiao Liang
Xiao Liang
You-Ting Zhu
You-Ting Zhu
You-Ting Zhu
Dan-Dan Feng
Dan-Dan Feng
Dan-Dan Feng
Sergey Dobretsov
Sergey Dobretsov
Jin-Long Yang
Jin-Long Yang
Jin-Long Yang
2(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscus
Frontiers in Marine Science
RNA-sequencing
furanone
marine bacterial biofilm
biofilm matrix
plantigrade settlement
Mytilus coruscus
title 2(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscus
title_full 2(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscus
title_fullStr 2(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscus
title_full_unstemmed 2(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscus
title_short 2(5H)-Furanone Disrupts Bacterial Biofilm Formation and Indirectly Reduces the Settlement of Plantigrades of the Mussel Mytilus coruscus
title_sort 2 5h furanone disrupts bacterial biofilm formation and indirectly reduces the settlement of plantigrades of the mussel mytilus coruscus
topic RNA-sequencing
furanone
marine bacterial biofilm
biofilm matrix
plantigrade settlement
Mytilus coruscus
url https://www.frontiersin.org/article/10.3389/fmars.2020.564075/full
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