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      Domain Shuffling in a Sensor Protein Contributed to the Evolution of Insect Pathogenicity in Plant-Beneficial Pseudomonas protegens

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          Abstract

          Pseudomonas protegens is a biocontrol rhizobacterium with a plant-beneficial and an insect pathogenic lifestyle, but it is not understood how the organism switches between the two states. Here, we focus on understanding the function and possible evolution of a molecular sensor that enables P. protegens to detect the insect environment and produce a potent insecticidal toxin specifically during insect infection but not on roots. By using quantitative single cell microscopy and mutant analysis, we provide evidence that the sensor histidine kinase FitF is a key regulator of insecticidal toxin production. Our experimental data and bioinformatic analyses indicate that FitF shares a sensing domain with DctB, a histidine kinase regulating carbon uptake in Proteobacteria. This suggested that FitF has acquired its specificity through domain shuffling from a common ancestor. We constructed a chimeric DctB-FitF protein and showed that it is indeed functional in regulating toxin expression in P. protegens. The shuffling event and subsequent adaptive modifications of the recruited sensor domain were critical for the microorganism to express its potent insect toxin in the observed host-specific manner. Inhibition of the FitF sensor during root colonization could explain the mechanism by which P. protegens differentiates between the plant and insect host. Our study establishes FitF of P. protegens as a prime model for molecular evolution of sensor proteins and bacterial pathogenicity.

          Author Summary

          Pseudomonas bacteria are well-known for their capability of adapting to different environments, which enables them to interact with various host organisms. Pseudomonas protegens is a plant-associated biocontrol bacterium with lifestyles that are of interest for agricultural applications, among them one as a competitive root colonizer protecting plants against pathogenic fungi and the other as an insect pathogen invading and killing insect species of importance as pests in agriculture. We recently discovered that P. protegens produces a potent insecticidal toxin only during infection of insects but not when growing on plant roots. Since sensor proteins enable bacteria to sense and respond to changing environments and are important for pathogen-host interactions, we investigated whether a specific sensory protein could explain our observation. We found that this particular protein tightly controls toxin production and during its evolution has recruited a common sensor domain from a regulatory protein involved in control of nutrient uptake. This so-called domain shuffling event was important for the ability of P. protegens to produce its insecticidal toxin only when it infects insects. Our study provides a prime example of how a sensory system can evolve and contribute to the evolution of bacterial pathogenicity.

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          Most cited references38

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          SMART, a simple modular architecture research tool: identification of signaling domains.

          Accurate multiple alignments of 86 domains that occur in signaling proteins have been constructed and used to provide a Web-based tool (SMART: simple modular architecture research tool) that allows rapid identification and annotation of signaling domain sequences. The majority of signaling proteins are multidomain in character with a considerable variety of domain combinations known. Comparison with established databases showed that 25% of our domain set could not be deduced from SwissProt and 41% could not be annotated by Pfam. SMART is able to determine the modular architectures of single sequences or genomes; application to the entire yeast genome revealed that at least 6.7% of its genes contain one or more signaling domains, approximately 350 greater than previously annotated. The process of constructing SMART predicted (i) novel domain homologues in unexpected locations such as band 4.1-homologous domains in focal adhesion kinases; (ii) previously unknown domain families, including a citron-homology domain; (iii) putative functions of domain families after identification of additional family members, for example, a ubiquitin-binding role for ubiquitin-associated domains (UBA); (iv) cellular roles for proteins, such predicted DEATH domains in netrin receptors further implicating these molecules in axonal guidance; (v) signaling domains in known disease genes such as SPRY domains in both marenostrin/pyrin and Midline 1; (vi) domains in unexpected phylogenetic contexts such as diacylglycerol kinase homologues in yeast and bacteria; and (vii) likely protein misclassifications exemplified by a predicted pleckstrin homology domain in a Candida albicans protein, previously described as an integrin.
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            Biological insights from structures of two-component proteins.

            Two-component signal transduction based on phosphotransfer from a histidine protein kinase to a response regulator protein is a prevalent strategy for coupling environmental stimuli to adaptive responses in bacteria. In both histidine kinases and response regulators, modular domains with conserved structures and biochemical activities adopt different conformational states in the presence of stimuli or upon phosphorylation, enabling a diverse array of regulatory mechanisms based on inhibitory and/or activating protein-protein interactions imparted by different domain arrangements. This review summarizes some of the recent structural work that has provided insight into the functioning of bacterial histidine kinases and response regulators. Particular emphasis is placed on identifying features that are expected to be conserved among different two-component proteins from those that are expected to differ, with the goal of defining the extent to which knowledge of previously characterized two-component proteins can be applied to newly discovered systems.
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              Evolution of two-component signal transduction systems.

              To exist in a wide range of environmental niches, bacteria must sense and respond to a variety of external signals. A primary means by which this occurs is through two-component signal transduction pathways, typically composed of a sensor histidine kinase that receives the input stimuli and then phosphorylates a response regulator that effects an appropriate change in cellular physiology. Histidine kinases and response regulators have an intrinsic modularity that separates signal input, phosphotransfer, and output response; this modularity has allowed bacteria to dramatically expand and diversify their signaling capabilities. Recent work has begun to reveal the molecular basis by which two-component proteins evolve. How and why do orthologous signaling proteins diverge? How do cells gain new pathways and recognize new signals? What changes are needed to insulate a new pathway from existing pathways? What constraints are there on gene duplication and lateral gene transfer? Here, we review progress made in answering these questions, highlighting how the integration of genome sequence data with experimental studies is providing major new insights.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                February 2014
                20 February 2014
                : 10
                : 2
                : e1003964
                Affiliations
                [1 ]Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
                [2 ]Plant Pathology, Institute of Integrative Biology, Swiss Federal Institute of Technology (ETH) Zurich, Zurich, Switzerland
                The University of North Carolina at Chapel Hill, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: PK CK. Performed the experiments: PK MPT NI. Analyzed the data: PK. Contributed reagents/materials/analysis tools: PK MPT NI MM CK. Wrote the paper: PK MM CK.

                Article
                PPATHOGENS-D-13-02452
                10.1371/journal.ppat.1003964
                3930604
                24586167
                08a209a6-c827-4bff-a212-de782b6e1c4d
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 19 September 2013
                : 16 January 2014
                Page count
                Pages: 15
                Funding
                This work was supported by the Swiss National Science Foundation ( www.snf.ch; grants no. 31003A_138248 and 406840_143141 NRP 68). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Evolutionary biology
                Evolutionary genetics
                Genetics
                Molecular genetics
                Gene identification and analysis
                Gene regulation
                Gene function
                Microbiology
                Bacterial pathogens
                Gram negative
                Host-pathogen interaction
                Microbial control
                Microbial evolution
                Microbial pathogens
                Plant microbiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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