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Antimicrobial and Insecticidal : cyclic lipopeptides and hydrogen cyanide produced by plant-beneficial Pseudomonas strains CHA0, CMR12a, and PCL1391 contribute to insect killing

Pascale Flury, Pilar Vesga, Maria Péchy-Tarr, Nora Aellen, Francesca Dennert, Nicolas Hofer, Karent P Kupferschmied, Peter Kupferschmied, Zane Metla, Zongwang Ma, et al. (2017) FRONTIERS IN MICROBIOLOGY. 8.
abstract
Particular groups of plant-beneficial fluorescent pseudomonads are not only root colonizers that provide plant disease suppression, but in addition are able to infect and kill insect larvae. The mechanisms by which the bacteria manage to infest this alternative host, to overcome its immune system, and to ultimately kill the insect are still largely unknown. However, the investigation of the few virulence factors discovered so far, points to a highly multifactorial nature of insecticidal activity. Antimicrobial compounds produced by fluorescent pseudomonads are effective weapons against a vast diversity of organisms such as fungi, oomycetes, nematodes, and protozoa. Here, we investigated whether these compounds also contribute to insecticidal activity. We tested mutants of the highly insecticidal strains Pseudomonas protegens CHA0, Pseudomonas chlororaphis PCL1391, and Pseudomonas sp. CMR12a, defective for individual or multiple antimicrobial compounds, for injectable and oral activity against lepidopteran insect larvae. Moreover, we studied expression of biosynthesis genes for these antimicrobial compounds for the first time in insects. Our survey revealed that hydrogen cyanide and different types of cyclic lipopeptides contribute to insecticidal activity. Hydrogen cyanide was essential to full virulence of CHA0 and PCL1391 directly injected into the hemolymph. The cyclic lipopeptide orfamide produced by CHA0 and CMR12a was mainly important in oral infections. Mutants of CMR12a and PCL1391 impaired in the production of the cyclic lipopeptides sessilin and clp 391, respectively, showed reduced virulence in injection and feeding experiments. Although virulence of mutants lacking one or several of the other antimicrobial compounds, i.e., 2,4-diacetylphloroglucinol, phenazines, pyrrolnitrin, or pyoluteorin, was not reduced, these metabolites might still play a role in an insect background since all investigated biosynthetic genes for antimicrobial compounds of strain CHA0 were expressed at some point during insect infection. In summary, our study identified new factors contributing to insecticidal activity and extends the diverse functions of antimicrobial compounds produced by fluorescent pseudomonads from the plant environment to the insect host.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
BLACK ROOT-ROT, GRAM-NEGATIVE BACTERIA, ENHANCED ANTIBIOTIC PRODUCTION, FLUORESCENS CHA0, BIOLOGICAL-CONTROL, DROSOPHILA-MELANOGASTER, GNOTOBIOTIC CONDITIONS, SECONDARY METABOLITES, PAENIBACILLUS-LARVAE, BIOCONTROL, orfamide, sessilin, Gac regulatory system, Pseudomonas fluorescens, Pseudomonas protegens, Pseudomonas chlororaphis, secondary metabolites, insecticidal activity
journal title
FRONTIERS IN MICROBIOLOGY
Front. Microbiol.
volume
8
article number
100
pages
15 pages
Web of Science type
Article
Web of Science id
000393219800001
ISSN
1664-302X
DOI
10.3389/fmicb.2017.00100
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
8512883
handle
http://hdl.handle.net/1854/LU-8512883
date created
2017-03-07 09:38:13
date last changed
2017-05-10 13:43:41
@article{8512883,
  abstract     = {Particular groups of plant-beneficial fluorescent pseudomonads are not only root colonizers that provide plant disease suppression, but in addition are able to infect and kill insect larvae. The mechanisms by which the bacteria manage to infest this alternative host, to overcome its immune system, and to ultimately kill the insect are still largely unknown. However, the investigation of the few virulence factors discovered so far, points to a highly multifactorial nature of insecticidal activity. Antimicrobial compounds produced by fluorescent pseudomonads are effective weapons against a vast diversity of organisms such as fungi, oomycetes, nematodes, and protozoa. Here, we investigated whether these compounds also contribute to insecticidal activity. We tested mutants of the highly insecticidal strains Pseudomonas protegens CHA0, Pseudomonas chlororaphis PCL1391, and Pseudomonas sp. CMR12a, defective for individual or multiple antimicrobial compounds, for injectable and oral activity against lepidopteran insect larvae. Moreover, we studied expression of biosynthesis genes for these antimicrobial compounds for the first time in insects. Our survey revealed that hydrogen cyanide and different types of cyclic lipopeptides contribute to insecticidal activity. Hydrogen cyanide was essential to full virulence of CHA0 and PCL1391 directly injected into the hemolymph. The cyclic lipopeptide orfamide produced by CHA0 and CMR12a was mainly important in oral infections. Mutants of CMR12a and PCL1391 impaired in the production of the cyclic lipopeptides sessilin and clp 391, respectively, showed reduced virulence in injection and feeding experiments. Although virulence of mutants lacking one or several of the other antimicrobial compounds, i.e., 2,4-diacetylphloroglucinol, phenazines, pyrrolnitrin, or pyoluteorin, was not reduced, these metabolites might still play a role in an insect background since all investigated biosynthetic genes for antimicrobial compounds of strain CHA0 were expressed at some point during insect infection. In summary, our study identified new factors contributing to insecticidal activity and extends the diverse functions of antimicrobial compounds produced by fluorescent pseudomonads from the plant environment to the insect host.},
  articleno    = {100},
  author       = {Flury, Pascale and Vesga, Pilar and P{\'e}chy-Tarr, Maria and Aellen, Nora and Dennert, Francesca and Hofer, Nicolas and Kupferschmied, Karent P and Kupferschmied, Peter and Metla, Zane and Ma, Zongwang and Siegfried, Sandra and de Weert, Sandra and Bloemberg, Guido and H{\"o}fte, Monica and Keel, Christoph J and Maurhofer, Monika},
  issn         = {1664-302X},
  journal      = {FRONTIERS IN MICROBIOLOGY},
  keyword      = {BLACK ROOT-ROT,GRAM-NEGATIVE BACTERIA,ENHANCED ANTIBIOTIC PRODUCTION,FLUORESCENS CHA0,BIOLOGICAL-CONTROL,DROSOPHILA-MELANOGASTER,GNOTOBIOTIC CONDITIONS,SECONDARY METABOLITES,PAENIBACILLUS-LARVAE,BIOCONTROL,orfamide,sessilin,Gac regulatory system,Pseudomonas fluorescens,Pseudomonas protegens,Pseudomonas chlororaphis,secondary metabolites,insecticidal activity},
  language     = {eng},
  pages        = {15},
  title        = {Antimicrobial and Insecticidal : cyclic lipopeptides and hydrogen cyanide produced by plant-beneficial Pseudomonas strains CHA0, CMR12a, and PCL1391 contribute to insect killing},
  url          = {http://dx.doi.org/10.3389/fmicb.2017.00100},
  volume       = {8},
  year         = {2017},
}

Chicago
Flury, Pascale, Pilar Vesga, Maria Péchy-Tarr, Nora Aellen, Francesca Dennert, Nicolas Hofer, Karent P Kupferschmied, et al. 2017. “Antimicrobial and Insecticidal : Cyclic Lipopeptides and Hydrogen Cyanide Produced by Plant-beneficial Pseudomonas Strains CHA0, CMR12a, and PCL1391 Contribute to Insect Killing.” Frontiers in Microbiology 8.
APA
Flury, P., Vesga, P., Péchy-Tarr, M., Aellen, N., Dennert, F., Hofer, N., Kupferschmied, K. P., et al. (2017). Antimicrobial and Insecticidal : cyclic lipopeptides and hydrogen cyanide produced by plant-beneficial Pseudomonas strains CHA0, CMR12a, and PCL1391 contribute to insect killing. FRONTIERS IN MICROBIOLOGY, 8.
Vancouver
1.
Flury P, Vesga P, Péchy-Tarr M, Aellen N, Dennert F, Hofer N, et al. Antimicrobial and Insecticidal : cyclic lipopeptides and hydrogen cyanide produced by plant-beneficial Pseudomonas strains CHA0, CMR12a, and PCL1391 contribute to insect killing. FRONTIERS IN MICROBIOLOGY. 2017;8.
MLA
Flury, Pascale, Pilar Vesga, Maria Péchy-Tarr, et al. “Antimicrobial and Insecticidal : Cyclic Lipopeptides and Hydrogen Cyanide Produced by Plant-beneficial Pseudomonas Strains CHA0, CMR12a, and PCL1391 Contribute to Insect Killing.” FRONTIERS IN MICROBIOLOGY 8 (2017): n. pag. Print.