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      Context-Specific Requirement of Forty-Four Two-Component Loci in Pseudomonas aeruginosa Swarming

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          Summary

          Swarming in Pseudomonas aeruginosa is a coordinated movement of bacteria over semisolid surfaces (0.5%–0.7% agar). On soft agar, P. aeruginosa exhibits a dendritic swarm pattern, with multiple levels of branching. However, the swarm patterns typically vary depending upon the experimental design. In the present study, we show that the pattern characteristics of P. aeruginosa swarm are highly environment dependent. We define several quantifiable, macroscale features of the swarm to study the plasticity of the swarm, observed across different nutrient formulations. Furthermore, through a targeted screen of 113 two-component system (TCS) loci of the P. aeruginosa strain PA14, we show that forty-four TCS genes regulate swarming in PA14 in a contextual fashion. However, only four TCS genes— fleR, fleS, gacS, and PA14_59770—were found essential for swarming. Notably, many swarming-defective TCS mutants were found highly efficient in biofilm formation, indicating opposing roles for many TCS loci.

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          Highlights

          • •

            The swarm pattern of Pseudomonas aeruginosa is plastic and growth media dependent

          • •

            P. aeruginosa swarming motility is promoted by nutrient limitation

          • •

            Forty-four P. aeruginosa genes encoding two-component system modulate swarming

          Abstract

          Pathogenic Organism; Biological Sciences; Microbiology

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          Most cited references44

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          Two-component signal transduction.

          A M Stock, V L Robinson, P Goudreau (2000)
          Most prokaryotic signal-transduction systems and a few eukaryotic pathways use phosphotransfer schemes involving two conserved components, a histidine protein kinase and a response regulator protein. The histidine protein kinase, which is regulated by environmental stimuli, autophosphorylates at a histidine residue, creating a high-energy phosphoryl group that is subsequently transferred to an aspartate residue in the response regulator protein. Phosphorylation induces a conformational change in the regulatory domain that results in activation of an associated domain that effects the response. The basic scheme is highly adaptable, and numerous variations have provided optimization within specific signaling systems. The domains of two-component proteins are modular and can be integrated into proteins and pathways in a variety of ways, but the core structures and activities are maintained. Thus detailed analyses of a relatively small number of representative proteins provide a foundation for understanding this large family of signaling proteins.
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            Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development.

            G. O'toole, R. Kolter (1998)
            The formation of complex bacterial communities known as biofilms begins with the interaction of planktonic cells with a surface in response to appropriate environmental signals. We report the isolation and characterization of mutants of Pseudomonas aeruginosa PA14 defective in the initiation of biofilm formation on an abiotic surface, polyvinylchloride (PVC) plastic. These mutants are designated surface attachment defective (sad ). Two classes of sad mutants were analysed: (i) mutants defective in flagellar-mediated motility and (ii) mutants defective in biogenesis of the polar-localized type IV pili. We followed the development of the biofilm formed by the wild type over 8 h using phase-contrast microscopy. The wild-type strain first formed a monolayer of cells on the abiotic surface, followed by the appearance of microcolonies that were dispersed throughout the monolayer of cells. Using time-lapse microscopy, we present evidence that microcolonies form by aggregation of cells present in the monolayer. As observed with the wild type, strains with mutations in genes required for the synthesis of type IV pili formed a monolayer of cells on the PVC plastic. However, in contrast to the wild-type strain, the type IV pili mutants did not develop microcolonies over the course of the experiments, suggesting that these structures play an important role in microcolony formation. Very few cells of a non-motile strain (carrying a mutation in flgK) attached to PVC even after 8 h of incubation, suggesting a role for flagella and/or motility in the initial cell-to-surface interactions. The phenotype of these mutants thus allows us to initiate the dissection of the developmental pathway leading to biofilm formation.
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              An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants.

              Nicole Liberati, Jonathan M. Urbach, Sachiko Miyata … (2006)
              Random transposon insertion libraries have proven invaluable in studying bacterial genomes. Libraries that approach saturation must be large, with multiple insertions per gene, making comprehensive genome-wide scanning difficult. To facilitate genome-scale study of the opportunistic human pathogen Pseudomonas aeruginosa strain PA14, we constructed a nonredundant library of PA14 transposon mutants (the PA14NR Set) in which nonessential PA14 genes are represented by a single transposon insertion chosen from a comprehensive library of insertion mutants. The parental library of PA14 transposon insertion mutants was generated by using MAR2xT7, a transposon compatible with transposon-site hybridization and based on mariner. The transposon-site hybridization genetic footprinting feature broadens the utility of the library by allowing pooled MAR2xT7 mutants to be individually tracked under different experimental conditions. A public, internet-accessible database (the PA14 Transposon Insertion Mutant Database, http://ausubellab.mgh.harvard.edu/cgi-bin/pa14/home.cgi) was developed to facilitate construction, distribution, and use of the PA14NR Set. The usefulness of the PA14NR Set in genome-wide scanning for phenotypic mutants was validated in a screen for attachment to abiotic surfaces. Comparison of the genes disrupted in the PA14 transposon insertion library with an independently constructed insertion library in P. aeruginosa strain PAO1 provides an estimate of the number of P. aeruginosa essential genes.
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                Author and article information

                Contributors
                Varsha Singh
                Journal
                Journal ID (nlm-ta): iScience
                Journal ID (iso-abbrev): iScience
                Title: iScience
                Publisher: Elsevier
                ISSN (Electronic): 2589-0042
                Publication date PMC-release: 01 March 2019
                Publication date Collection: 29 March 2019
                Publication date (Electronic): 01 March 2019
                Volume: 13
                Pages: 305-317
                Affiliations
                [1 ]Department of Molecular Reproduction, Development and Genetics, Indian Institute of Science, Bangalore, Karnataka 560012, India
                [2 ]Centre for Nano Science and Engineering, Indian Institute of Science, Bangalore, Karnataka 560012, India
                [3 ]Biosystems Science and Engineering, Indian Institute of Science, Bangalore, Karnataka 560012, India
                [4 ]Robert Bosch Centre for Cyber Physical Systems, Indian Institute of Science, Bangalore, Karnataka 560012, India
                Author notes
                [∗ ]Corresponding author varsha@ 123456iisc.ac.in
                [5]

                These authors contributed equally

                [6]

                Lead Contact

                Article
                Publisher ID: S2589-0042(19)30062-8
                DOI: 10.1016/j.isci.2019.02.028
                PMC ID: 6423354
                PubMed ID: 30877999
                SO-VID: a809f5c1-e3ae-4dc6-9118-6e0c9255835e
                Copyright © © 2019 The Authors
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 26 October 2018
                Date revision received : 18 December 2018
                Date accepted : 26 February 2019
                Categories
                Subject: Article

                Keywords: pathogenic organism,biological sciences,microbiology
                Data availability:
                Keywords: pathogenic organism, biological sciences, microbiology

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