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      Feedback regulation of Caulobacter crescentus holdfast synthesis by flagellum assembly via the holdfast inhibitor HfiA : Caulobacter holdfast regulation by flagellum assembly

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          Abstract

          <p id="P3">To permanently attach to surfaces, <i>Caulobacter crescentus</i> produces a strong adhesive, the holdfast. The timing of holdfast synthesis is developmentally regulated by cell cycle cues. When <i>C. crescentus</i> is grown in a complex medium, holdfast synthesis can also be stimulated by surface sensing, in which swarmer cells rapidly synthesize holdfast in direct response to surface contact. In contrast to growth in complex medium, here we show that when cells are grown in a defined medium, surface contact does not trigger holdfast synthesis. Moreover, we show that in a defined medium, flagellum synthesis and regulation of holdfast production are linked. In these conditions, mutants lacking a flagellum attach to surfaces over time more efficiently than either wild-type strains or strains harboring a paralyzed flagellum. Enhanced adhesion in mutants lacking flagellar components is due to premature holdfast synthesis during the cell cycle and is regulated by the holdfast synthesis inhibitor HfiA. <i>hfiA</i> transcription is reduced in flagellar mutants and this reduction is modulated by the diguanylate cyclase developmental regulator PleD. We also show that, in contrast to previous predictions, flagella are not necessarily required for <i>C. crescentus</i> surface sensing in the absence of flow, and that arrest of flagellar rotation does not stimulate holdfast synthesis. Rather, our data support a model in which flagellum assembly feeds back to control holdfast synthesis via HfiA expression in a c-di-GMP dependent manner under defined nutrient conditions. </p><p class="first" id="P4"> <i>Caulobacter crescentus</i> produces a strong adhesive, the holdfast, to permanently attach to surfaces and form biofilms. In this study, we show that flagellum assembly is developmentally connected to the production of holdfast dependent upon both nutrient availability and c-di-GMP. These results provide new insight into the regulation of single cell adhesion and initial surface colonization leading to the process of biofilm formation. </p><p id="P5"> <div class="figure-container so-text-align-c"> <img alt="" class="figure" src="/document_file/1d1d0819-32f3-484b-a094-491f32033d02/PubMedCentral/image/nihms-984019-f0001.jpg"/> </div> </p>

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          Most cited references47

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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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            MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis

            Single cell analysis of bacteria and subcellular protein localization dynamics has shown that bacteria have elaborate life cycles, cytoskeletal protein networks, and complex signal transduction pathways driven by localized proteins. The volume of multi-dimensional images generated in such experiments and the computation time required to detect, associate, and track cells and subcellular features pose considerable challenges, especially for high-throughput experiments. Therefore, there is a need for a versatile, computationally efficient image analysis tool capable of extracting the desired relationships from images in a meaningful and unbiased way. Here we present MicrobeJ, a plug-in for the open-source platform ImageJ. MicrobeJ provides a comprehensive framework to process images derived from a wide variety of microscopy experiments with special emphasis on large image sets. It performs the most common intensity and morphology measurements as well as customized detection of poles, septa, fluorescent foci, and organelles, determines their sub-cellular localization with sub-pixel resolution, and tracks them over time. Because a dynamic link is maintained between the images, measurements, and all data representations derived from them, the editor and suite of advanced data presentation tools facilitates the image analysis process and provides a robust way to verify the accuracy and veracity of the data.
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              Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor.

              High levels of the intracellular signalling molecule cyclic diguanylate (c-di-GMP) supress motility and activate exopolysaccharide (EPS) production in a variety of bacterial species. In many bacteria part of the effect of c-di-GMP is on gene expression, but the mechanism involved is not known for any species. We have identified the protein FleQ as a c-di-GMP-responsive transcriptional regulator in Pseudomonas aeruginosa. FleQ is known to activate expression of flagella biosynthesis genes. Here we show that it also represses transcription of genes including the pel operon involved in EPS biosynthesis, and that this repression is relieved by c-di-GMP. Our in vivo data indicate that FleQ represses pel transcription and that pel transcription is not repressed when intracellular c-di-GMP levels are high. FleN, a known antiactivator of FleQ also participates in control of pel expression. In in vitro experiments we found that FleQ binds to pel promoter DNA and that this binding is inhibited by c-di-GMP. FleQ binds radiolabelled c-di-GMP in vitro. FleQ does not have amino acid motifs that resemble previously defined c-di-GMP binding domains. Our results show that FleQ is a new type of c-di-GMP binding protein that controls the transcriptional regulation of EPS biosynthesis genes in P. aeruginosa.
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                Author and article information

                Journal
                Molecular Microbiology
                Molecular Microbiology
                Wiley
                0950382X
                October 2018
                October 2018
                October 05 2018
                : 110
                : 2
                : 219-238
                Affiliations
                [1 ]Department of Biology; Indiana University; 1001 E. 3rd Street Bloomington IN 47405 USA
                [2 ]Department of Genetics; Harvard Medical School; Boston MA 02115 USA
                [3 ]Department of Biochemistry and Molecular Biology; Michigan State University; East Lansing MI USA
                [4 ]Department of Biochemistry and Molecular Biology; University of Chicago; Chicago IL USA
                [5 ]Department of Microbiology and Molecular Genetics; Michigan State University; East Lansing MI USA
                Article
                10.1111/mmi.14099
                6195837
                30079982
                ace23c5a-6b91-43d0-8471-5bb30f291fc3
                © 2018

                http://doi.wiley.com/10.1002/tdm_license_1.1

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