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      Stress responses go three dimensional – the spatial order of physiological differentiation in bacterial macrocolony biofilms

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      Environmental Microbiology
      BlackWell Publishing Ltd

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          Abstract

          In natural habitats, bacteria often occur in multicellular communities characterized by a robust extracellular matrix of proteins, amyloid fibres, exopolysaccharides and extracellular DNA. These biofilms show pronounced stress resistance including a resilience against antibiotics that causes serious medical and technical problems. This review summarizes recent studies that have revealed clear spatial physiological differentiation, complex supracellular architecture and striking morphology in macrocolony biofilms. By responding to gradients of nutrients, oxygen, waste products and signalling compounds that build up in growing biofilms, various stress responses determine whether bacteria grow and proliferate or whether they enter into stationary phase and use their remaining resources for maintenance and survival. As a consequence, biofilms differentiate into at least two distinct layers of vegetatively growing and stationary phase cells that exhibit very different cellular physiology. This includes a stratification of matrix production with a major impact on microscopic architecture, biophysical properties and directly visible morphology of macrocolony biofilms. Using E scherichia coli as a model system, this review also describes our detailed current knowledge about the underlying molecular control networks – prominently featuring sigma factors, transcriptional cascades and second messengers – that drive this spatial differentiation and points out directions for future research.

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          Most cited references124

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          Physiological heterogeneity in biofilms.

          Biofilms contain bacterial cells that are in a wide range of physiological states. Within a biofilm population, cells with diverse genotypes and phenotypes that express distinct metabolic pathways, stress responses and other specific biological activities are juxtaposed. The mechanisms that contribute to this genetic and physiological heterogeneity include microscale chemical gradients, adaptation to local environmental conditions, stochastic gene expression and the genotypic variation that occurs through mutation and selection. Here, we discuss the processes that generate chemical gradients in biofilms, the genetic and physiological responses of the bacteria as they adapt to these gradients and the techniques that can be used to visualize and measure the microscale physiological heterogeneities of bacteria in biofilms.
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            Fruiting body formation by Bacillus subtilis.

            Spore formation by the bacterium Bacillus subtilis has long been studied as a model for cellular differentiation, but predominantly as a single cell. When analyzed within the context of highly structured, surface-associated communities (biofilms), spore formation was discovered to have heretofore unsuspected spatial organization. Initially, motile cells differentiated into aligned chains of attached cells that eventually produced aerial structures, or fruiting bodies, that served as preferential sites for sporulation. Fruiting body formation depended on regulatory genes required early in sporulation and on genes evidently needed for exopolysaccharide and surfactin production. The formation of aerial structures was robust in natural isolates but not in laboratory strains, an indication that multicellularity has been lost during domestication of B. subtilis. Other microbial differentiation processes long thought to involve only single cells could display the spatial organization characteristic of multicellular organisms when studied with recent natural isolates.
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              Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili.

              We have used Escherichia coli as a model system to investigate the initiation of biofilm formation. Here, we demonstrate that E. coli forms biofilms on multiple abiotic surfaces in a nutrient-dependent fashion. In addition, we have isolated insertion mutations that render this organism defective in biofilm formation. One-half of these mutations was found to perturb normal flagellar function. Using defined fli, flh, mot and che alleles, we show that motility, but not chemotaxis, is critical for normal biofilm formation. Microscopic analyses of these mutants suggest that motility is important for both initial interaction with the surface and for movement along the surface. In addition, we present evidence that type I pili (harbouring the mannose-specific adhesin, FimH) are required for initial surface attachment and that mannose inhibits normal attachment. In light of the observations presented here, a working model is discussed that describes the roles of both motility and type I pili in biofilm development.
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                Author and article information

                Journal
                Environ Microbiol
                Environ. Microbiol
                emi
                Environmental Microbiology
                BlackWell Publishing Ltd (Oxford, UK )
                1462-2912
                1462-2920
                June 2014
                05 May 2014
                : 16
                : 6
                : 1455-1471
                Affiliations
                Institute of Biology/Microbiology, Humboldt Universität zu Berlin Chausseestr. 117, Berlin, 10115, Germany
                Author notes
                *For correspondence. E-mail regine.hengge@ 123456hu-berlin.de ; Tel. (49) 30 2093 8101; Fax (49) 30 2093 8102.
                Article
                10.1111/1462-2920.12483
                4238805
                24725389
                7fd5cdf2-35f8-453e-a6ac-80527c04a936
                Copyright © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd

                This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

                History
                : 22 January 2014
                : 28 March 2014
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                Microbiology & Virology
                Microbiology & Virology

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