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      De novo evolved interference competition promotes the spread of biofilm defectors

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          Abstract

          Biofilms are social entities where bacteria live in tightly packed agglomerations, surrounded by self-secreted exopolymers. Since production of exopolymers is costly and potentially exploitable by non-producers, mechanisms that prevent invasion of non-producing mutants are hypothesized. Here we study long-term dynamics and evolution in Bacillus subtilis biofilm populations consisting of wild-type (WT) matrix producers and mutant non-producers. We show that non-producers initially fail to incorporate into biofilms formed by the WT cells, resulting in 100-fold lower final frequency compared to the WT. However, this is modulated in a long-term scenario, as non-producers evolve the ability to better incorporate into biofilms, thereby slightly decreasing the productivity of the whole population. Detailed molecular analysis reveals that the unexpected shift in the initially stable biofilm is coupled with newly evolved phage-mediated interference competition. Our work therefore demonstrates how collective behaviour can be disrupted as a result of rapid adaptation through mobile genetic elements.

          Abstract

          The production of secreted polymers in bacterial biofilms is costly, and therefore mechanisms preventing invasion of non-producing mutants are hypothesized. Here, the authors show that non-producers can evolve the ability to better incorporate into biofilms via phage-mediated interference.

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          Microbial biofilms.

          Direct observations have clearly shown that biofilm bacteria predominate, numerically and metabolically, in virtually all nutrient-sufficient ecosystems. Therefore, these sessile organisms predominate in most of the environmental, industrial, and medical problems and processes of interest to microbiologists. If biofilm bacteria were simply planktonic cells that had adhered to a surface, this revelation would be unimportant, but they are demonstrably and profoundly different. We first noted that biofilm cells are at least 500 times more resistant to antibacterial agents. Now we have discovered that adhesion triggers the expression of a sigma factor that derepresses a large number of genes so that biofilm cells are clearly phenotypically distinct from their planktonic counterparts. Each biofilm bacterium lives in a customized microniche in a complex microbial community that has primitive homeostasis, a primitive circulatory system, and metabolic cooperativity, and each of these sessile cells reacts to its special environment so that it differs fundamentally from a planktonic cell of the same species.
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            The tragedy of the commons. The population problem has no technical solution; it requires a fundamental extension in morality.

            G. Hardin (1968)
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              Adaptive radiation in a heterogeneous environment.

              Successive adaptive radiations have played a pivotal role in the evolution of biological diversity. The effects of adaptive radiation are often seen, but the underlying causes are difficult to disentangle and remain unclear. Here we examine directly the role of ecological opportunity and competition in driving genetic diversification. We use the common aerobic bacterium Pseudomonas fluorescens, which evolves rapidly under novel environmental conditions to generate a large repertoire of mutants. When provided with ecological opportunity (afforded by spatial structure), identical populations diversify morphologically, but when ecological opportunity is restricted there is no such divergence. In spatially structured environments, the evolution of variant morphs follows a predictable sequence and we show that competition among the newly evolved niche-specialists maintains this variation. These results demonstrate that the elementary processes of mutation and selection alone are sufficient to promote rapid proliferation of new designs and support the theory that trade-offs in competitive ability drive adaptive radiation.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                02 May 2017
                2017
                : 8
                : 15127
                Affiliations
                [1 ]Terrestrial Biofilms Group, Institute of Microbiology, Friedrich Schiller University Jena , Jena 07743, Germany
                [2 ]Institute of Biochemistry, Biological Research Centre, Hungarian Academy of Sciences , Szeged 6726, Hungary
                [3 ]Seqomics Biotechnology Ltd. , Mórahalom 6782, Hungary
                [4 ]Electron Microscopy Center, Jena University Hospital , Jena 07743, Germany
                Author notes
                [*]

                These authors contributed equally to this work.

                Article
                ncomms15127
                10.1038/ncomms15127
                5418572
                28462927
                fb34f7e8-89e8-41e5-9e13-9f018a911834
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 05 October 2016
                : 02 March 2017
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