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      We Are One: Multispecies Metabolism of a Biofilm Consortium and Their Treatment Strategies

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          Abstract

          The ecological and medical significance of bacterial biofilms have been well recognized. Biofilms are harder to control than their planktonic free-living counterparts and quite recently, the focus of the study has shifted to the multispecies consortia, which represent the vast majority of real-case infection scenarios. Studies have begun to explore the complex interspecies interactions within these biofilms. However, only little attention is currently given to the role of cellular metabolites in the cell-to-cell communication. The concentration gradients of metabolic substrates and products affect the spatial growth of bacteria in multispecies biofilm. This, if looked into more deeply, can lead to identification of potential therapies targeting the specific metabolites and hence the coordinated protection in the bacterial community. Herein, we review the interspecies communications, including their metabolic cross-talking, in multispecies biofilm, to signify the importance of such interactions on the initial formation and subsequent growth of these biofilms. Multispecies biofilms with their species heterogeneity are more resilient to antimicrobial agents than their single species biofilm counterparts and this characteristic is of particular interest when dealing with pathogenic bacteria. In this Review, we also discuss the treatment options available, to include current and emerging avenues to combat pathogenic multispecies biofilms in the clinical, environmental, as well as industrial settings.

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          Most cited references81

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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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            Oral multispecies biofilm development and the key role of cell-cell distance.

            Growth of oral bacteria in situ requires adhesion to a surface because the constant flow of host secretions thwarts the ability of planktonic cells to grow before they are swallowed. Therefore, oral bacteria evolved to form biofilms on hard tooth surfaces and on soft epithelial tissues, which often contain multiple bacterial species. Because these biofilms are easy to study, they have become the paradigm of multispecies biofilms. In this Review we describe the factors involved in the formation of these biofilms, including the initial adherence to the oral tissues and teeth, cooperation between bacterial species in the biofilm, signalling between the bacteria and its role in pathogenesis, and the transfer of DNA between bacteria. In all these aspects distance between cells of different species is integral for oral biofilm growth.
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              Bacteria and archaea on Earth and their abundance in biofilms

              Biofilms are a form of collective life with emergent properties that confer many advantages on their inhabitants, and they represent a much higher level of organization than single cells do. However, to date, no global analysis on biofilm abundance exists. We offer a critical discussion of the definition of biofilms and compile current estimates of global cell numbers in major microbial habitats, mindful of the associated uncertainty. Most bacteria and archaea on Earth (1.2 × 1030 cells) exist in the 'big five' habitats: deep oceanic subsurface (4 × 1029), upper oceanic sediment (5 × 1028), deep continental subsurface (3 × 1029), soil (3 × 1029) and oceans (1 × 1029). The remaining habitats, including groundwater, the atmosphere, the ocean surface microlayer, humans, animals and the phyllosphere, account for fewer cells by orders of magnitude. Biofilms dominate in all habitats on the surface of the Earth, except in the oceans, accounting for ~80% of bacterial and archaeal cells. In the deep subsurface, however, they cannot always be distinguished from single sessile cells; we estimate that 20-80% of cells in the subsurface exist as biofilms. Hence, overall, 40-80% of cells on Earth reside in biofilms. We conclude that biofilms drive all biogeochemical processes and represent the main way of active bacterial and archaeal life.
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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
                28 January 2021
                2021
                : 12
                : 635432
                Affiliations
                [1] 1iThree Institute, University of Technology Sydney , Sydney, NSW, Australia
                [2] 2School of Chemical Engineering, University of New South Wales , Sydney, NSW, Australia
                Author notes

                Edited by: Enrica Pessione, University of Turin, Italy

                Reviewed by: Giuliana Banche, University of Turin, Italy; Ilana Kolodkin-Gal, Weizmann Institute of Science, Israel

                *Correspondence: Riti Mann, Riti.Mann@ 123456uts.edu.au

                These authors have contributed equally to this work

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

                Article
                10.3389/fmicb.2021.635432
                7876221
                33584635
                ce30d03a-aa2d-45f3-80e9-faeaf810e16e
                Copyright © 2021 Joshi, Gunawan and Mann.

                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 November 2020
                : 11 January 2021
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 81, Pages: 9, Words: 0
                Funding
                Funded by: Australian Research Council 10.13039/501100000923
                Categories
                Microbiology
                Mini Review

                Microbiology & Virology
                biofilms,multispecies,metabolism,treatment,interactions
                Microbiology & Virology
                biofilms, multispecies, metabolism, treatment, interactions

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