Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil

ABSTRACT Potatoes are cultivated in southwest Greenland without the use of pesticides and with limited crop rotation. Despite the fact that plant-pathogenic fungi are present, no severe-disease outbreaks have yet been observed. In this report, we document that a potato soil at Inneruulalik in southe...

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Autores principales:	Charlotte F. Michelsen, Jeramie Watrous, Mikkel A. Glaring, Roland Kersten, Nobuhiro Koyama, Pieter C. Dorrestein, Peter Stougaard
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/770318b39738478189e3b4455a66f80f
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spelling	oai:doaj.org-article:770318b39738478189e3b4455a66f80f2021-11-15T15:41:33ZNonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil10.1128/mBio.00079-152150-7511https://doaj.org/article/770318b39738478189e3b4455a66f80f2015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00079-15https://doaj.org/toc/2150-7511ABSTRACT Potatoes are cultivated in southwest Greenland without the use of pesticides and with limited crop rotation. Despite the fact that plant-pathogenic fungi are present, no severe-disease outbreaks have yet been observed. In this report, we document that a potato soil at Inneruulalik in southern Greenland is suppressive against Rhizoctonia solani Ag3 and uncover the suppressive antifungal mechanism of a highly potent biocontrol bacterium, Pseudomonas fluorescens In5, isolated from the suppressive potato soil. A combination of molecular genetics, genomics, and matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) imaging mass spectrometry (IMS) revealed an antifungal genomic island in P. fluorescens In5 encoding two nonribosomal peptides, nunamycin and nunapeptin, which are key components for the biocontrol activity by strain In5 in vitro and in soil microcosm experiments. Furthermore, complex microbial behaviors were highlighted. Whereas nunamycin was demonstrated to inhibit the mycelial growth of R. solani Ag3, but not that of Pythium aphanidermatum, nunapeptin instead inhibited P. aphanidermatum but not R. solani Ag3. Moreover, the synthesis of nunamycin by P. fluorescens In5 was inhibited in the presence of P. aphanidermatum. Further characterization of the two peptides revealed nunamycin to be a monochlorinated 9-amino-acid cyclic lipopeptide with similarity to members of the syringomycin group, whereas nunapeptin was a 22-amino-acid cyclic lipopeptide with similarity to corpeptin and syringopeptin. IMPORTANCE Crop rotation and systematic pest management are used to only a limited extent in Greenlandic potato farming. Nonetheless, although plant-pathogenic fungi are present in the soil, the farmers do not experience major plant disease outbreaks. Here, we show that a Greenlandic potato soil is suppressive against Rhizoctonia solani, and we unravel the key biocontrol components for Pseudomonas fluorescens In5, one of the potent biocontrol bacteria isolated from this Greenlandic suppressive soil. Using a combination of molecular genetics, genomics, and microbial imaging mass spectrometry, we show that two cyclic lipopeptides, nunamycin and nunapeptin, are important for the biocontrol activity of P. fluorescens In5 both in vitro and in microcosm assays. Furthermore, we demonstrate that the synthesis of nunamycin is repressed by the oomycete Pythium aphanidermatum. Overall, our report provides important insight into interkingdom interference between bacteria and fungi/oomycetes.Charlotte F. MichelsenJeramie WatrousMikkel A. GlaringRoland KerstenNobuhiro KoyamaPieter C. DorresteinPeter StougaardAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Charlotte F. Michelsen Jeramie Watrous Mikkel A. Glaring Roland Kersten Nobuhiro Koyama Pieter C. Dorrestein Peter Stougaard Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil
description	ABSTRACT Potatoes are cultivated in southwest Greenland without the use of pesticides and with limited crop rotation. Despite the fact that plant-pathogenic fungi are present, no severe-disease outbreaks have yet been observed. In this report, we document that a potato soil at Inneruulalik in southern Greenland is suppressive against Rhizoctonia solani Ag3 and uncover the suppressive antifungal mechanism of a highly potent biocontrol bacterium, Pseudomonas fluorescens In5, isolated from the suppressive potato soil. A combination of molecular genetics, genomics, and matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) imaging mass spectrometry (IMS) revealed an antifungal genomic island in P. fluorescens In5 encoding two nonribosomal peptides, nunamycin and nunapeptin, which are key components for the biocontrol activity by strain In5 in vitro and in soil microcosm experiments. Furthermore, complex microbial behaviors were highlighted. Whereas nunamycin was demonstrated to inhibit the mycelial growth of R. solani Ag3, but not that of Pythium aphanidermatum, nunapeptin instead inhibited P. aphanidermatum but not R. solani Ag3. Moreover, the synthesis of nunamycin by P. fluorescens In5 was inhibited in the presence of P. aphanidermatum. Further characterization of the two peptides revealed nunamycin to be a monochlorinated 9-amino-acid cyclic lipopeptide with similarity to members of the syringomycin group, whereas nunapeptin was a 22-amino-acid cyclic lipopeptide with similarity to corpeptin and syringopeptin. IMPORTANCE Crop rotation and systematic pest management are used to only a limited extent in Greenlandic potato farming. Nonetheless, although plant-pathogenic fungi are present in the soil, the farmers do not experience major plant disease outbreaks. Here, we show that a Greenlandic potato soil is suppressive against Rhizoctonia solani, and we unravel the key biocontrol components for Pseudomonas fluorescens In5, one of the potent biocontrol bacteria isolated from this Greenlandic suppressive soil. Using a combination of molecular genetics, genomics, and microbial imaging mass spectrometry, we show that two cyclic lipopeptides, nunamycin and nunapeptin, are important for the biocontrol activity of P. fluorescens In5 both in vitro and in microcosm assays. Furthermore, we demonstrate that the synthesis of nunamycin is repressed by the oomycete Pythium aphanidermatum. Overall, our report provides important insight into interkingdom interference between bacteria and fungi/oomycetes.
format	article
author	Charlotte F. Michelsen Jeramie Watrous Mikkel A. Glaring Roland Kersten Nobuhiro Koyama Pieter C. Dorrestein Peter Stougaard
author_facet	Charlotte F. Michelsen Jeramie Watrous Mikkel A. Glaring Roland Kersten Nobuhiro Koyama Pieter C. Dorrestein Peter Stougaard
author_sort	Charlotte F. Michelsen
title	Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil
title_short	Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil
title_full	Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil
title_fullStr	Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil
title_full_unstemmed	Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil
title_sort	nonribosomal peptides, key biocontrol components for <named-content content-type="genus-species">pseudomonas fluorescens</named-content> in5, isolated from a greenlandic suppressive soil
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/770318b39738478189e3b4455a66f80f
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Nonribosomal Peptides, Key Biocontrol Components for <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> In5, Isolated from a Greenlandic Suppressive Soil

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