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      N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities

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          Abstract

          Bacterial biofilms are important medically, environmentally and industrially and there is a need to understand the processes that govern functional synergy and dynamics of species within biofilm communities. Here, we have used a model, mixed-species biofilm community comprised of Pseudomonas aeruginosa PAO1, Pseudomonas protegens Pf-5 and Klebsiella pneumoniae KP1. This biofilm community displays higher biomass and increased resilience to antimicrobial stress conditions such as sodium dodecyl sulfate and tobramycin, compared to monospecies biofilm populations. P. aeruginosa is present at low proportions in the community and yet, it plays a critical role in community function, suggesting it acts as a keystone species in this community. To determine the factors that regulate community composition, we focused on P. aeruginosa because of its pronounced impact on community structure and function. Specifically, we evaluated the role of the N-acyl homoserine lactone (AHL) dependent quorum sensing (QS) system of P. aeruginosa PAO1, which regulates group behaviors including biofilm formation and the production of effector molecules. We found that mixed species biofilms containing P. aeruginosa QS mutants had significantly altered proportions of K. pneumoniae and P. protegens populations compared to mixed species biofilms with the wild type P. aeruginosa. Similarly, inactivation of QS effector genes, e.g. rhlA and pvdR, also governed the relative species proportions. While the absence of QS did not alter the proportions of the two species in dual species biofilms of P. aeruginosa and K. pneumoniae, it resulted in significantly lower proportions of P. aeruginosa in dual species biofilms with P. protegens. These observations suggest that QS plays an important role in modulating community biofilm structure and physiology and affects interspecific interactions.

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          Most cited references74

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          The biofilm matrix.

          The microorganisms in biofilms live in a self-produced matrix of hydrated extracellular polymeric substances (EPS) that form their immediate environment. EPS are mainly polysaccharides, proteins, nucleic acids and lipids; they provide the mechanical stability of biofilms, mediate their adhesion to surfaces and form a cohesive, three-dimensional polymer network that interconnects and transiently immobilizes biofilm cells. In addition, the biofilm matrix acts as an external digestive system by keeping extracellular enzymes close to the cells, enabling them to metabolize dissolved, colloidal and solid biopolymers. Here we describe the functions, properties and constituents of the EPS matrix that make biofilms the most successful forms of life on earth.
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            Biofilms: an emergent form of bacterial life.

            Bacterial biofilms are formed by communities that are embedded in a self-produced matrix of extracellular polymeric substances (EPS). Importantly, bacteria in biofilms exhibit a set of 'emergent properties' that differ substantially from free-living bacterial cells. In this Review, we consider the fundamental role of the biofilm matrix in establishing the emergent properties of biofilms, describing how the characteristic features of biofilms - such as social cooperation, resource capture and enhanced survival of exposure to antimicrobials - all rely on the structural and functional properties of the matrix. Finally, we highlight the value of an ecological perspective in the study of the emergent properties of biofilms, which enables an appreciation of the ecological success of biofilms as habitat formers and, more generally, as a bacterial lifestyle.
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              Multistate point-prevalence survey of health care-associated infections.

              Currently, no single U.S. surveillance system can provide estimates of the burden of all types of health care-associated infections across acute care patient populations. We conducted a prevalence survey in 10 geographically diverse states to determine the prevalence of health care-associated infections in acute care hospitals and generate updated estimates of the national burden of such infections. We defined health care-associated infections with the use of National Healthcare Safety Network criteria. One-day surveys of randomly selected inpatients were performed in participating hospitals. Hospital personnel collected demographic and limited clinical data. Trained data collectors reviewed medical records retrospectively to identify health care-associated infections active at the time of the survey. Survey data and 2010 Nationwide Inpatient Sample data, stratified according to patient age and length of hospital stay, were used to estimate the total numbers of health care-associated infections and of inpatients with such infections in U.S. acute care hospitals in 2011. Surveys were conducted in 183 hospitals. Of 11,282 patients, 452 had 1 or more health care-associated infections (4.0%; 95% confidence interval, 3.7 to 4.4). Of 504 such infections, the most common types were pneumonia (21.8%), surgical-site infections (21.8%), and gastrointestinal infections (17.1%). Clostridium difficile was the most commonly reported pathogen (causing 12.1% of health care-associated infections). Device-associated infections (i.e., central-catheter-associated bloodstream infection, catheter-associated urinary tract infection, and ventilator-associated pneumonia), which have traditionally been the focus of programs to prevent health care-associated infections, accounted for 25.6% of such infections. We estimated that there were 648,000 patients with 721,800 health care-associated infections in U.S. acute care hospitals in 2011. Results of this multistate prevalence survey of health care-associated infections indicate that public health surveillance and prevention activities should continue to address C. difficile infections. As device- and procedure-associated infections decrease, consideration should be given to expanding surveillance and prevention activities to include other health care-associated infections.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/1071720
                URI : https://loop.frontiersin.org/people/1247792
                URI : https://loop.frontiersin.org/people/214601
                URI : https://loop.frontiersin.org/people/1065193
                URI : https://loop.frontiersin.org/people/150099
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                18 March 2021
                2021
                : 11
                : 646991
                Affiliations
                [1] 1 Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University , Singapore, Singapore
                [2] 2 School of Biological Sciences, Nanyang Technological University , Singapore, Singapore
                [3] 3 ithree Institute, The University of Technology Sydney , Sydney, NSW, Australia
                Author notes

                Edited by: Mingkai Li, Fourth Military Medical University, China

                Reviewed by: William Schwan, University of Wisconsin–La Crosse, United States; Wayne Heaselgrave, University of Wolverhampton, United Kingdom

                *Correspondence: Scott A. Rice, rscott@ 123456ntu.edu.sg

                This article was submitted to Clinical Microbiology, a section of the journal Frontiers in Cellular and Infection Microbiology

                Article
                10.3389/fcimb.2021.646991
                8044998
                33869078
                bcedf74d-45c0-47c1-9cd1-c36706ae7300
                Copyright © 2021 Subramoni, Muzaki, Booth, Kjelleberg and Rice

                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.

                History
                : 28 December 2020
                : 25 February 2021
                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 74, Pages: 16, Words: 9058
                Funding
                Funded by: Ministry of Education - Singapore 10.13039/501100001459
                Award ID: MOE2019-T2-1-050
                Categories
                Cellular and Infection Microbiology
                Original Research

                Infectious disease & Microbiology
                quorum sensing,species interactions,multispecies,biofilms,pseudomonas aeruginosa,pseudomonas protegens,klebsiella pneumoniae

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