Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.

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. proteg...

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Autores principales:	Peter Kupferschmied, Maria Péchy-Tarr, Nicola Imperiali, Monika Maurhofer, Christoph Keel
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/d7387a896eea41f682d3ce3031f5a05d
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spelling	oai:doaj.org-article:d7387a896eea41f682d3ce3031f5a05d2021-11-18T06:06:57ZDomain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.1553-73661553-737410.1371/journal.ppat.1003964https://doaj.org/article/d7387a896eea41f682d3ce3031f5a05d2014-02-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24586167/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Pseudomonas 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.Peter KupferschmiedMaria Péchy-TarrNicola ImperialiMonika MaurhoferChristoph KeelPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 10, Iss 2, p e1003964 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Peter Kupferschmied Maria Péchy-Tarr Nicola Imperiali Monika Maurhofer Christoph Keel Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.
description	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.
format	article
author	Peter Kupferschmied Maria Péchy-Tarr Nicola Imperiali Monika Maurhofer Christoph Keel
author_facet	Peter Kupferschmied Maria Péchy-Tarr Nicola Imperiali Monika Maurhofer Christoph Keel
author_sort	Peter Kupferschmied
title	Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.
title_short	Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.
title_full	Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.
title_fullStr	Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.
title_full_unstemmed	Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens.
title_sort	domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial pseudomonas protegens.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/d7387a896eea41f682d3ce3031f5a05d
work_keys_str_mv	AT peterkupferschmied domainshufflinginasensorproteincontributedtotheevolutionofinsectpathogenicityinplantbeneficialpseudomonasprotegens AT mariapechytarr domainshufflinginasensorproteincontributedtotheevolutionofinsectpathogenicityinplantbeneficialpseudomonasprotegens AT nicolaimperiali domainshufflinginasensorproteincontributedtotheevolutionofinsectpathogenicityinplantbeneficialpseudomonasprotegens AT monikamaurhofer domainshufflinginasensorproteincontributedtotheevolutionofinsectpathogenicityinplantbeneficialpseudomonasprotegens AT christophkeel domainshufflinginasensorproteincontributedtotheevolutionofinsectpathogenicityinplantbeneficialpseudomonasprotegens
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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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