Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein

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 volt...

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Autores principales:	Liang Wu, Regina S. McGrane, Gwyn A. Beattie
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/11cc9ec4b08b491cb460a3f4870b3a6b
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spelling	oai:doaj.org-article:11cc9ec4b08b491cb460a3f4870b3a6b2021-11-15T15:40:05ZLight Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein10.1128/mBio.00334-132150-7511https://doaj.org/article/11cc9ec4b08b491cb460a3f4870b3a6b2013-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00334-13https://doaj.org/toc/2150-7511ABSTRACT 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.Liang WuRegina S. McGraneGwyn A. BeattieAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 3 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Liang Wu Regina S. McGrane Gwyn A. Beattie Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein
description	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.
format	article
author	Liang Wu Regina S. McGrane Gwyn A. Beattie
author_facet	Liang Wu Regina S. McGrane Gwyn A. Beattie
author_sort	Liang Wu
title	Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein
title_short	Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein
title_full	Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein
title_fullStr	Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein
title_full_unstemmed	Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein
title_sort	light regulation of swarming motility in <named-content content-type="genus-species">pseudomonas syringae</named-content> integrates signaling pathways mediated by a bacteriophytochrome and a lov protein
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/11cc9ec4b08b491cb460a3f4870b3a6b
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Light Regulation of Swarming Motility in <named-content content-type="genus-species">Pseudomonas syringae</named-content> Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein

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