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Environmental Microbiology

Fungal-Associated Molecules Induce Key Genes Involved in the Biosynthesis of the Antifungal Secondary Metabolites Nunamycin and Nunapeptin in the Biocontrol Strain Pseudomonas fluorescens In5

Line Christiansen, Katrine Skov Alanin, Christopher B. W. Phippen, Stefan Olsson, Peter Stougaard, Rosanna C. Hennessy
Rebecca E. Parales, Editor
Line Christiansen
aDepartment of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark
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Katrine Skov Alanin
aDepartment of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark
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Christopher B. W. Phippen
bDepartment of Biotechnology and Biomedicine, Technical University of Denmark, Lyngby, Denmark
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Stefan Olsson
cState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou City, Fujian Province, China
dPlant Immunity Center, Haixia Institute of Science and Technology, College of Life Science, Fujian Agriculture and Forestry University, Fuzhou City, Fujian Province, China
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Peter Stougaard
eDepartment of Environmental Science, Aarhus University, Roskilde, Denmark
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Rosanna C. Hennessy
aDepartment of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark
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Rebecca E. Parales
University of California, Davis
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DOI: 10.1128/AEM.01284-20
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ABSTRACT

Pseudomonas fluorescens In5 synthesizes the antifungal cyclic lipopeptides (CLPs) nunamycin and nunapeptin, which are similar in structure and genetic organization to the pseudomonas-derived phytotoxins syringomycin and syringopeptin. Regulation of syringomycin and syringopeptin is dependent on the two-component global regulatory system GacS-GacA and the SalA, SyrF, and SyrG transcription factors, which activate syringomycin synthesis in response to plant signal molecules. Previously, we demonstrated that a specific transcription factor, NunF, positively regulates the synthesis of nunamycin and nunapeptin in P. fluorescens In5 and that the nunF gene is upregulated by fungal-associated molecules. This study focused on further unravelling the complex regulation governing CLP synthesis in P. fluorescens In5. Promoter fusions were used to show that the specific activator NunF is dependent on the global regulator of secondary metabolism GacA and is regulated by fungal-associated molecules and low temperatures. In contrast, GacA is stimulated by plant signal molecules leading to the hypothesis that P. fluorescens is a hyphosphere-associated bacterium carrying transcription factor genes that respond to signals indicating the presence of fungi and oomycetes. Based on these findings, we present a model for how synthesis of nunamycin and nunapeptin is regulated by fungal- and oomycete-associated molecules.

IMPORTANCE Cyclic lipopeptide (CLP) synthesis gene clusters in pseudomonads display a high degree of synteny, and the structures of the peptides synthesized are very similar. Accordingly, the genomic island encoding the synthesis of syringomycin and syringopeptin in P. syringae pv. syringae closely resembles that of P. fluorescens In5, which contains genes coding for synthesis of the antifungal and anti-oomycete peptides nunamycin and nunapeptin, respectively. However, the regulation of syringomycin and syringopeptin synthesis is different from that of nunamycin and nunapeptin synthesis. While CLP synthesis in the plant pathogen P. syringae pv. syringae is induced by plant signal molecules, such compounds do not significantly influence synthesis of nunamycin and nunapeptin in P. fluorescens In5. Instead, fungal-associated molecules positively regulate antifungal peptide synthesis in P. fluorescens In5, while the synthesis of the global regulator GacA in P. fluorescens In5 is positively regulated by plant signal molecules but not fungal-associated molecules.

FOOTNOTES

    • Received 29 May 2020.
    • Accepted 12 August 2020.
    • Accepted manuscript posted online 21 August 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Fungal-Associated Molecules Induce Key Genes Involved in the Biosynthesis of the Antifungal Secondary Metabolites Nunamycin and Nunapeptin in the Biocontrol Strain Pseudomonas fluorescens In5
Line Christiansen, Katrine Skov Alanin, Christopher B. W. Phippen, Stefan Olsson, Peter Stougaard, Rosanna C. Hennessy
Applied and Environmental Microbiology Oct 2020, 86 (21) e01284-20; DOI: 10.1128/AEM.01284-20

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Fungal-Associated Molecules Induce Key Genes Involved in the Biosynthesis of the Antifungal Secondary Metabolites Nunamycin and Nunapeptin in the Biocontrol Strain Pseudomonas fluorescens In5
Line Christiansen, Katrine Skov Alanin, Christopher B. W. Phippen, Stefan Olsson, Peter Stougaard, Rosanna C. Hennessy
Applied and Environmental Microbiology Oct 2020, 86 (21) e01284-20; DOI: 10.1128/AEM.01284-20
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KEYWORDS

gene fusions
gene regulation
lipopeptides
natural antimicrobial products
Pseudomonas
secondary metabolites
biocontrol

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