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      Exopolysaccharide composition and size in Sulfolobus acidocaldarius biofilms

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          Abstract

          Extracellular polymeric substances (EPS) comprise mainly carbohydrates, proteins and extracellular DNA (eDNA) in biofilms formed by the thermoacidophilic Crenarchaeon Sulfolobus acidocaldarius. However, detailed information on the carbohydrates in the S. acidocaldarius biofilm EPS, i.e., the exopolysaccharides (PS), in terms of identity, composition and size were missing. In this study, a set of methods was developed and applied to study the PS in S. acidocaldarius biofilms. It was initially shown that addition of sugars, most significantly of glucose, to the basal N-Z-amine-based growth medium enhanced biofilm formation. For the generation of sufficient amounts of biomass suitable for chemical analyses, biofilm growth was established and optimized on the surface of membrane filters. EPS were isolated and the contents of carbohydrates, proteins and eDNA were determined. PS purification was achieved by enzymatic digestion of other EPS components (nucleic acids and proteins). After trifluoroacetic acid-mediated hydrolysis of the PS fraction, the monosaccharide composition was analyzed by reversed-phase liquid chromatography (RP-LC) coupled to mass spectrometry (MS). Main sugar constituents detected were mannose, glucose and ribose, as well as minor proportions of rhamnose, N-acetylglucosamine, glucosamine and galactosamine. Size exclusion chromatography (SEC) revealed the presence of one single PS fraction with a molecular mass of 4-9 × 10 4 Da. This study provides detailed information on the PS composition and size of S. acidocaldarius MW001 biofilms and methodological tools for future studies on PS biosynthesis and secretion.

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          Most cited references75

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          Colorimetric Method for Determination of Sugars and Related Substances

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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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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                26 September 2022
                2022
                : 13
                : 982745
                Affiliations
                [1] 1Molecular Enzyme Technology and Biochemistry, Environmental Microbiology and Biotechnology, Centre for Water and Environmental Research, University of Duisburg-Essen , Essen, Germany
                [2] 2Applied Analytical Chemistry, University of Duisburg-Essen , Essen, Germany
                [3] 3Teaching and Research Center for Separation, University of Duisburg-Essen , Essen, Germany
                [4] 4Aquatic Microbiology, Environmental Microbiology and Biotechnology, Centre for Water and Environmental Research, University of Duisburg-Essen , Essen, Germany
                Author notes

                Edited by: Dennis W. Grogan, University of Cincinnati, United States

                Reviewed by: Andrea Koerdt, Federal Institute for Materials Research and Testing (BAM), Germany; Maria Michela Corsaro, University of Naples Federico II, Italy

                *Correspondence: Bettina Siebers, bettina.siebers@ 123456uni-due.de

                These authors have contributed equally to this work and share first authorship

                ORCID: Martin Meyer, orcid.org/0000-0002-7360-1849; Jost Wingender, orcid.org/0000-0003-3143-4760; Oliver J. Schmitz, orcid.org/0000-0003-2184-1207; Bettina Siebers, orcid.org/0000-0002-9905-541X

                This article was submitted to Biology of Archaea, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2022.982745
                9549778
                36225367
                699468f9-300b-472e-a89d-da070216720f
                Copyright © 2022 Kuschmierz, Meyer, Bräsen, Wingender, Schmitz and Siebers.

                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
                : 30 June 2022
                : 30 August 2022
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 75, Pages: 16, Words: 11803
                Funding
                Funded by: Deutsche Forschungsgemeinschaft , doi 10.13039/501100001659;
                Award ID: SCHM 1699/26-1
                Award ID: SI 642/13-1
                Award ID: WI 831/4-1
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                sulfolobus acidocaldarius,archaea,biofilm,extracellular polymeric substances,exopolysaccharide,reversed-phase liquid chromatography,size exclusion chromatography

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