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      Light Regulation of Swarming Motility in Pseudomonas syringae Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein

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      mBio
      American Society of Microbiology

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          ABSTRACT

          The biological and regulatory roles of photosensory proteins are poorly understood for nonphotosynthetic bacteria. The foliar bacterial pathogen Pseudomonas syringae has three photosensory protein-encoding genes that are predicted to encode the blue-light-sensing LOV (light, oxygen, or voltage) histidine kinase (LOV-HK) and two red/far-red-light-sensing bacteriophytochromes, BphP1 and BphP2. We provide evidence that LOV-HK and BphP1 form an integrated network that regulates swarming motility in response to multiple light wavelengths. The swarming motility of P. syringae B728a deletion mutants indicated that LOV-HK positively regulates swarming motility in response to blue light and BphP1 negatively regulates swarming motility in response to red and far-red light. BphP2 does not detectably regulate swarming motility. The histidine kinase activity of each LOV-HK and BphP1 is required for this regulation based on the loss of complementation upon mutation of residues key to their kinase activity. Surprisingly, mutants lacking both lov and bphP1 were similar in motility to a bphP1 single mutant in blue light, indicating that the loss of bphP1 is epistatic to the loss of lov and also that BphP1 unexpectedly responds to blue light. Moreover, whereas expression of bphP1 did not alter motility under blue light in a bphP1 mutant, it reduced motility in a mutant lacking lov and bphP1, demonstrating that LOV-HK positively regulates motility by suppressing negative regulation by BphP1. These results are the first to show cross talk between the LOV protein and phytochrome signaling pathways in bacteria, and the similarity of this regulatory network to that of photoreceptors in plants suggests a possible common ancestry.

          IMPORTANCE

          Photosensory proteins enable organisms to perceive and respond to light. The biological and ecological roles of these proteins in nonphotosynthetic bacteria are largely unknown. This study discovered that a blue-light-sensing LOV (light, oxygen, or voltage) protein and a red/far-red-light-sensing bacteriophytochrome both regulate swarming motility in the foliar pathogen Pseudomonas syringae. These proteins form an integrated signaling network in which the bacteriophytochrome represses swarming motility in response to red, far-red, and blue light, and LOV positively regulates swarming motility by suppressing bacteriophytochrome-mediated blue-light signaling. This is the first example of cross talk between LOV and phytochrome signaling pathways in bacteria, which shows unexpected similarity to photoreceptor signaling in plants.

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          Most cited references48

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans.

            pRK212.2, a derivative of the broad host range plasmid RK2, contains two EcoRI cleavage fragments, A and B, neither of which can replicate by itself in Escherichia coli. Fragment A (41.7 kilobases), but not fragment B (14.4 kilobases), can be cloned by insertion into the unrelated plasmids mini-F and ColE1. Fragment B contains the origin of replication and the ampicillin-resistance determinant of RK2. Transformation of E. coli cells containing the mini-F-fragment A hybrid plasmid with fragment B DNA results in the recircularization and replication of fragment B as a nonmobilizable plasmid (pRK2067) with the copy number and incompatibility properties of RK2. Fragment B cannot be cloned in the absence of fragment A because the latter fragment suppresses a function, specified by fragment B, that results in loss of host cell viability. A small segment (2.4 kilobases) of fragment B that contains the RK2 origin of replication but no longer affects host cell growth in the absence of fragment A had been cloned previously by insertion into a ColE1 plasmid. This hybrid plasmid, designated pRK256, will replicate in E. coli polA mutants only when a fragment A-bearing helper plasmid is present. These results demonstrate that the potentially lethal function specified by fragment B of RK2 is not necessary for replication and that at least one trans-acting function is directly involved in RK2 replication.
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              Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria.

              A new group of photoreceptors has been experimentally revealed in cyanobacteria. They are phototaxis regulator SyPixJ1, TePixJ and AnPixJ, chromatic acclimation regulator SyCcaS, circadian input kinase homolog SyCikA and many other candidates, which have been found only in cyanobacteria to date. These new photoreceptors are now proposed to be "cyanobacteriochromes". They are characterized by the presence of a chromophore-binding GAF domain that is homologous to the tetrapyrrole-binding GAF domain of the phytochrome. Here, we summarized unique features of those representatives: (1) only the GAF domain is sufficient for full photoconversion, (2) the GAF domain is homologous to but distinct from the phytochrome GAF, (3) the GAF domain binds a linear tetrapyrrole pigment such as phycoviolobilin or phycocyanobilin, (4) spectral properties are very diverse from near ultra-violet to red region. We also discussed the functionality of the other candidate GAFs, structure and evolution.
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                Author and article information

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society of Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                11 June 2013
                May-Jun 2013
                : 4
                : 3
                : e00334-13
                Affiliations
                [1]Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, USA
                Author notes
                Address correspondence to Gwyn A. Beattie, gbeattie@ 123456iastate.edu .

                Editor E. Peter Greenberg, University of Washington

                Article
                mBio00334-13
                10.1128/mBio.00334-13
                3684834
                23760465
                abd83092-cda0-488c-8796-a657b79d98e6
                Copyright © 2013 Wu et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 2 May 2013
                : 20 May 2013
                Page count
                Pages: 9
                Categories
                Research Article
                Custom metadata
                May/June 2013

                Life sciences
                Life sciences

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