Insect pathogenicity in plant-beneficial pseudomonads: phylogenetic distribution and comparative genomics

Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties including pathogen suppression. Recent observations that some strains of this group also cause lethal infections in insect larvae, however,...

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Published in:The ISME Journal Vol. 10; no. 10; pp. 2527 - 2542
Main Authors: Flury, Pascale, Aellen, Nora, Ruffner, Beat, Péchy-Tarr, Maria, Fataar, Shakira, Metla, Zane, Dominguez-Ferreras, Ana, Bloemberg, Guido, Frey, Joachim, Goesmann, Alexander, Raaijmakers, Jos M, Duffy, Brion, Höfte, Monica, Blom, Jochen, Smits, Theo H M, Keel, Christoph, Maurhofer, Monika
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 01.10.2016
Oxford University Press
Nature Publishing Group
Subjects:
45
45/23
45/70
631/208/212
631/326/171/1818
631/326/41/2531
Agricultural practices
Animals
Biomedical and Life Sciences
Ecology
Evolutionary Biology
Genomics
Host Specificity
Insects
Integrated pest management
Larva - microbiology
Larvae
Lepidoptera
Lepidoptera - microbiology
Life Sciences
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Original
original-article
Pathogens
Pest control
Phylogeny
Plants - microbiology
Pseudomonas
Pseudomonas - genetics
Pseudomonas - isolation & purification
Pseudomonas - pathogenicity
Pseudomonas - physiology
Pseudomonas chlororaphis
Pseudomonas fluorescens
Virulence
ISSN:1751-7362, 1751-7370, 1751-7370
Online Access:Get full text
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Abstract Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties including pathogen suppression. Recent observations that some strains of this group also cause lethal infections in insect larvae, however, point to a more versatile ecology of these bacteria. We show that 26 P. fluorescens group strains, isolated from three continents and covering three phylogenetically distinct sub-clades, exhibited different activities toward lepidopteran larvae, ranging from lethal to avirulent. All strains of sub-clade 1, which includes Pseudomonas chlororaphis and Pseudomonas protegens , were highly insecticidal regardless of their origin (animals, plants). Comparative genomics revealed that strains in this sub-clade possess specific traits allowing a switch between plant- and insect-associated lifestyles. We identified 90 genes unique to all highly insecticidal strains (sub-clade 1) and 117 genes common to all strains of sub-clade 1 and present in some moderately insecticidal strains of sub-clade 3. Mutational analysis of selected genes revealed the importance of chitinase C and phospholipase C in insect pathogenicity. The study provides insight into the genetic basis and phylogenetic distribution of traits defining insecticidal activity in plant-beneficial pseudomonads. Strains with potent dual activity against plant pathogens and herbivorous insects have great potential for use in integrated pest management for crops.
AbstractList Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties including pathogen suppression. Recent observations that some strains of this group also cause lethal infections in insect larvae, however, point to a more versatile ecology of these bacteria. We show that 26 P. fluorescens group strains, isolated from three continents and covering three phylogenetically distinct sub-clades, exhibited different activities toward lepidopteran larvae, ranging from lethal to avirulent. All strains of sub-clade 1, which includes Pseudomonas chlororaphis and Pseudomonas protegens, were highly insecticidal regardless of their origin (animals, plants). Comparative genomics revealed that strains in this sub-clade possess specific traits allowing a switch between plant- and insect-associated lifestyles. We identified 90 genes unique to all highly insecticidal strains (sub-clade 1) and 117 genes common to all strains of sub-clade 1 and present in some moderately insecticidal strains of sub-clade 3. Mutational analysis of selected genes revealed the importance of chitinase C and phospholipase C in insect pathogenicity. The study provides insight into the genetic basis and phylogenetic distribution of traits defining insecticidal activity in plant-beneficial pseudomonads. Strains with potent dual activity against plant pathogens and herbivorous insects have great potential for use in integrated pest management for crops.
Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties including pathogen suppression. Recent observations that some strains of this group also cause lethal infections in insect larvae, however, point to a more versatile ecology of these bacteria. We show that 26 P. fluorescens group strains, isolated from three continents and covering three phylogenetically distinct sub-clades, exhibited different activities toward lepidopteran larvae, ranging from lethal to avirulent. All strains of sub-clade 1, which includes Pseudomonas chlororaphis and Pseudomonas protegens, were highly insecticidal regardless of their origin (animals, plants). Comparative genomics revealed that strains in this sub-clade possess specific traits allowing a switch between plant- and insect-associated lifestyles. We identified 90 genes unique to all highly insecticidal strains (sub-clade 1) and 117 genes common to all strains of sub-clade 1 and present in some moderately insecticidal strains of sub-clade 3. Mutational analysis of selected genes revealed the importance of chitinase C and phospholipase C in insect pathogenicity. The study provides insight into the genetic basis and phylogenetic distribution of traits defining insecticidal activity in plant-beneficial pseudomonads. Strains with potent dual activity against plant pathogens and herbivorous insects have great potential for use in integrated pest management for crops.Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties including pathogen suppression. Recent observations that some strains of this group also cause lethal infections in insect larvae, however, point to a more versatile ecology of these bacteria. We show that 26 P. fluorescens group strains, isolated from three continents and covering three phylogenetically distinct sub-clades, exhibited different activities toward lepidopteran larvae, ranging from lethal to avirulent. All strains of sub-clade 1, which includes Pseudomonas chlororaphis and Pseudomonas protegens, were highly insecticidal regardless of their origin (animals, plants). Comparative genomics revealed that strains in this sub-clade possess specific traits allowing a switch between plant- and insect-associated lifestyles. We identified 90 genes unique to all highly insecticidal strains (sub-clade 1) and 117 genes common to all strains of sub-clade 1 and present in some moderately insecticidal strains of sub-clade 3. Mutational analysis of selected genes revealed the importance of chitinase C and phospholipase C in insect pathogenicity. The study provides insight into the genetic basis and phylogenetic distribution of traits defining insecticidal activity in plant-beneficial pseudomonads. Strains with potent dual activity against plant pathogens and herbivorous insects have great potential for use in integrated pest management for crops.
Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties including pathogen suppression. Recent observations that some strains of this group also cause lethal infections in insect larvae, however, point to a more versatile ecology of these bacteria. We show that 26 P. fluorescens group strains, isolated from three continents and covering three phylogenetically distinct sub-clades, exhibited different activities toward lepidopteran larvae, ranging from lethal to avirulent. All strains of sub-clade 1, which includes Pseudomonas chlororaphis and Pseudomonas protegens , were highly insecticidal regardless of their origin (animals, plants). Comparative genomics revealed that strains in this sub-clade possess specific traits allowing a switch between plant- and insect-associated lifestyles. We identified 90 genes unique to all highly insecticidal strains (sub-clade 1) and 117 genes common to all strains of sub-clade 1 and present in some moderately insecticidal strains of sub-clade 3. Mutational analysis of selected genes revealed the importance of chitinase C and phospholipase C in insect pathogenicity. The study provides insight into the genetic basis and phylogenetic distribution of traits defining insecticidal activity in plant-beneficial pseudomonads. Strains with potent dual activity against plant pathogens and herbivorous insects have great potential for use in integrated pest management for crops.
Author Aellen, Nora
Metla, Zane
Dominguez-Ferreras, Ana
Blom, Jochen
Flury, Pascale
Ruffner, Beat
Péchy-Tarr, Maria
Maurhofer, Monika
Raaijmakers, Jos M
Fataar, Shakira
Goesmann, Alexander
Duffy, Brion
Frey, Joachim
Bloemberg, Guido
Höfte, Monica
Smits, Theo H M
Keel, Christoph
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  organization: Plant Pathology, Institute of Integrative Biology, ETH Zürich
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  surname: Aellen
  fullname: Aellen, Nora
  organization: Plant Pathology, Institute of Integrative Biology, ETH Zürich
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  givenname: Beat
  surname: Ruffner
  fullname: Ruffner, Beat
  organization: Plant Pathology, Institute of Integrative Biology, ETH Zürich
– sequence: 4
  givenname: Maria
  surname: Péchy-Tarr
  fullname: Péchy-Tarr, Maria
  organization: Department of Fundamental Microbiology, University of Lausanne
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  givenname: Shakira
  surname: Fataar
  fullname: Fataar, Shakira
  organization: Plant Pathology, Institute of Integrative Biology, ETH Zürich
– sequence: 6
  givenname: Zane
  surname: Metla
  fullname: Metla, Zane
  organization: Plant Pathology, Institute of Integrative Biology, ETH Zürich, Laboratory of Experimental Entomology, Institute of Biology, University of Latvia
– sequence: 7
  givenname: Ana
  surname: Dominguez-Ferreras
  fullname: Dominguez-Ferreras, Ana
  organization: Plant Pathology, Institute of Integrative Biology, ETH Zürich
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  givenname: Guido
  surname: Bloemberg
  fullname: Bloemberg, Guido
  organization: Institute of Medical Microbiology, University of Zurich
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  givenname: Joachim
  surname: Frey
  fullname: Frey, Joachim
  organization: Institute of Veterinary Bacteriology, University of Bern
– sequence: 10
  givenname: Alexander
  surname: Goesmann
  fullname: Goesmann, Alexander
  organization: Bioinformatics and Systems Biology, Justus-Liebig-University Giessen
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  organization: Department of Microbial Ecology, Netherlands Institute of Ecology, NIOO-KNAW
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  givenname: Brion
  surname: Duffy
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  organization: Environmental Genomics and Systems Biology Research Group, Institute for Natural Resource Sciences, Zürich University of Applied Sciences
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  givenname: Monica
  surname: Höfte
  fullname: Höfte, Monica
  organization: Laboratory of Phytopathology, Faculty of Bioscience Engineering, Ghent University
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  surname: Blom
  fullname: Blom, Jochen
  organization: Bioinformatics and Systems Biology, Justus-Liebig-University Giessen
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  givenname: Theo H M
  surname: Smits
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  email: theo.smits@zhaw.ch
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  organization: Plant Pathology, Institute of Integrative Biology, ETH Zürich
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26894448$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright International Society for Microbial Ecology 2016
Copyright Nature Publishing Group Oct 2016
Copyright © 2016 International Society for Microbial Ecology 2016 International Society for Microbial Ecology
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Snippet Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties...
Bacteria of the genus Pseudomonas occupy diverse environments. The Pseudomonas fluorescens group is particularly well-known for its plant-beneficial properties...
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StartPage 2527
SubjectTerms 45
45/23
45/70
631/208/212
631/326/171/1818
631/326/41/2531
Agricultural practices
Animals
Biomedical and Life Sciences
Ecology
Evolutionary Biology
Genomics
Host Specificity
Insects
Integrated pest management
Larva - microbiology
Larvae
Lepidoptera
Lepidoptera - microbiology
Life Sciences
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Original
original-article
Pathogens
Pest control
Phylogeny
Plants - microbiology
Pseudomonas
Pseudomonas - genetics
Pseudomonas - isolation & purification
Pseudomonas - pathogenicity
Pseudomonas - physiology
Pseudomonas chlororaphis
Pseudomonas fluorescens
Virulence
Title Insect pathogenicity in plant-beneficial pseudomonads: phylogenetic distribution and comparative genomics
URI https://link.springer.com/article/10.1038/ismej.2016.5
https://www.ncbi.nlm.nih.gov/pubmed/26894448
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https://pubmed.ncbi.nlm.nih.gov/PMC5030700
Volume 10
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