Convection and the Extracellular Matrix Dictate Inter- and Intra-Biofilm Quorum Sensing Communication in Environmental Systems
The mechanisms and impact of bacterial quorum sensing (QS) for the coordination of population-level behaviors are well studied under laboratory conditions. However, it is unclear how, in otherwise open environmental systems, QS signals accumulate to sufficient concentration to induce QS phenotypes,...
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| Vydané v: | Environmental science & technology Ročník 54; číslo 11; s. 6730 |
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| Hlavní autori: | , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
02.06.2020
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| ISSN: | 1520-5851, 1520-5851 |
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| Abstract | The mechanisms and impact of bacterial quorum sensing (QS) for the coordination of population-level behaviors are well studied under laboratory conditions. However, it is unclear how, in otherwise open environmental systems, QS signals accumulate to sufficient concentration to induce QS phenotypes, especially when quorum quenching (QQ) organisms are also present. We explore the impact of QQ activity on QS signaling in spatially organized biofilms in scenarios that mimic open systems of natural and engineered environments. Using a functionally differentiated biofilm system, we show that the extracellular matrix, local flow, and QQ interact to modulate communication. In still aqueous environments, convection facilitates signal dispersal while the matrix absorbs and relays signals to the cells. This process facilitates inter-biofilm communication even at low extracellular signal concentrations. Within the biofilm, the matrix further regulates the transport of the competing QS and QQ molecules, leading to heterogenous QS behavior. Importantly, only extracellular QQ enzymes can effectively control QS signaling, suggesting that the intracellular QQ enzymes may not have evolved to degrade environmental QS signals for competition. |
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| AbstractList | The mechanisms and impact of bacterial quorum sensing (QS) for the coordination of population-level behaviors are well studied under laboratory conditions. However, it is unclear how, in otherwise open environmental systems, QS signals accumulate to sufficient concentration to induce QS phenotypes, especially when quorum quenching (QQ) organisms are also present. We explore the impact of QQ activity on QS signaling in spatially organized biofilms in scenarios that mimic open systems of natural and engineered environments. Using a functionally differentiated biofilm system, we show that the extracellular matrix, local flow, and QQ interact to modulate communication. In still aqueous environments, convection facilitates signal dispersal while the matrix absorbs and relays signals to the cells. This process facilitates inter-biofilm communication even at low extracellular signal concentrations. Within the biofilm, the matrix further regulates the transport of the competing QS and QQ molecules, leading to heterogenous QS behavior. Importantly, only extracellular QQ enzymes can effectively control QS signaling, suggesting that the intracellular QQ enzymes may not have evolved to degrade environmental QS signals for competition.The mechanisms and impact of bacterial quorum sensing (QS) for the coordination of population-level behaviors are well studied under laboratory conditions. However, it is unclear how, in otherwise open environmental systems, QS signals accumulate to sufficient concentration to induce QS phenotypes, especially when quorum quenching (QQ) organisms are also present. We explore the impact of QQ activity on QS signaling in spatially organized biofilms in scenarios that mimic open systems of natural and engineered environments. Using a functionally differentiated biofilm system, we show that the extracellular matrix, local flow, and QQ interact to modulate communication. In still aqueous environments, convection facilitates signal dispersal while the matrix absorbs and relays signals to the cells. This process facilitates inter-biofilm communication even at low extracellular signal concentrations. Within the biofilm, the matrix further regulates the transport of the competing QS and QQ molecules, leading to heterogenous QS behavior. Importantly, only extracellular QQ enzymes can effectively control QS signaling, suggesting that the intracellular QQ enzymes may not have evolved to degrade environmental QS signals for competition. The mechanisms and impact of bacterial quorum sensing (QS) for the coordination of population-level behaviors are well studied under laboratory conditions. However, it is unclear how, in otherwise open environmental systems, QS signals accumulate to sufficient concentration to induce QS phenotypes, especially when quorum quenching (QQ) organisms are also present. We explore the impact of QQ activity on QS signaling in spatially organized biofilms in scenarios that mimic open systems of natural and engineered environments. Using a functionally differentiated biofilm system, we show that the extracellular matrix, local flow, and QQ interact to modulate communication. In still aqueous environments, convection facilitates signal dispersal while the matrix absorbs and relays signals to the cells. This process facilitates inter-biofilm communication even at low extracellular signal concentrations. Within the biofilm, the matrix further regulates the transport of the competing QS and QQ molecules, leading to heterogenous QS behavior. Importantly, only extracellular QQ enzymes can effectively control QS signaling, suggesting that the intracellular QQ enzymes may not have evolved to degrade environmental QS signals for competition. |
| Author | Tan, Chuan Hao Sloot, Peter M A Kjelleberg, Staffan Oh, Hyun-Suk Sheraton, Vivek M Mancini, Emiliano Rice, Scott A Joachim Loo, Say Chye |
| Author_xml | – sequence: 1 givenname: Chuan Hao surname: Tan fullname: Tan, Chuan Hao organization: School of Materials Science and Engineering, Nanyang Technological University, 637551, Singapore – sequence: 2 givenname: Hyun-Suk orcidid: 0000-0002-9398-199X surname: Oh fullname: Oh, Hyun-Suk organization: Department of Environmental Engineering, Seoul National University of Science and Technology, 01811 Seoul, South Korea – sequence: 3 givenname: Vivek M surname: Sheraton fullname: Sheraton, Vivek M organization: Complexity Institute, Nanyang Technological University, 639798, Singapore – sequence: 4 givenname: Emiliano surname: Mancini fullname: Mancini, Emiliano organization: Institute for Advanced Study, University of Amsterdam, 1012 GC Amsterdam, The Netherlands – sequence: 5 givenname: Say Chye orcidid: 0000-0001-5300-1275 surname: Joachim Loo fullname: Joachim Loo, Say Chye organization: School of Materials Science and Engineering, Nanyang Technological University, 637551, Singapore – sequence: 6 givenname: Staffan surname: Kjelleberg fullname: Kjelleberg, Staffan organization: Centre for Marine Bio-Innovation, The Schools of Biotechnology and Biomolecular Sciences, and Biological, Earth and Environmental Sciences, University of New South Wales, 2031 Sydney, Australia – sequence: 7 givenname: Peter M A surname: Sloot fullname: Sloot, Peter M A organization: ITMO University, 197101 St. Petersburg, Russian Federation – sequence: 8 givenname: Scott A orcidid: 0000-0002-9486-2343 surname: Rice fullname: Rice, Scott A organization: The ithree Institute, University of Technology Sydney, 2007 Sydney, Australia |
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