Biosynthesis of the antimicrobial cyclic lipopeptides nunamycin and nunapeptin by <i>Pseudomonas fluorescens</i> strain In5 is regulated by the LuxR‐type transcriptional regulator NunF

Hennessy, Rosanna C.; Phippen, Christopher B. W.; Nielsen, Kristian Fog; Olsson, Stefan; Stougaard, Peter

doi:10.1002/mbo3.516

Cited by 29 publications

(29 citation statements)

References 63 publications

(99 reference statements)

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“…A complex regulatory cascade composed of, in the order of hierarchy, SalA, SyrG, and SyrF, activates expression of the syp/syr genes (Wang, Lu, Records, et al 2006;Wang, Lu, Yang, et al 2006;Vaughn and Gross 2016). Likewise, the syrF homolog, nunF, is required for production of both nunamycin and nunapeptin (Hennessy et al 2017). An homologous regulator, braD, is also conserved in the P. corrugata group but at a slightly shifted position, downstream the brabantamide operon.…”

Section: A Plethora Of Lp-associated Luxr Regulatorsmentioning

confidence: 99%

Lipopeptide families at the interface between pathogenic and beneficialPseudomonas-plant interactions

Girard

Höfte

Mot

2020

Critical Reviews in Microbiology

106

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Lipopeptides (LPs) are a prominent class of molecules among the steadily growing spectrum of specialized metabolites retrieved from Pseudomonas, in particular soil-dwelling and plant-associated isolates. Among the multiple LP families, pioneering research focussed on phytotoxic and antimicrobial cyclic lipopeptides (CLPs) of the ubiquitous plant pathogen Pseudomonas syringae (syringomycin and syringopeptin). Their non-ribosomal peptide synthetases (NRPSs) are embedded in biosynthetic gene clusters (BGCs) that are tightly co-clustered on a pathogenicity island. Other members of the P. syringae group (Pseudomonas cichorii) and some species of the Pseudomonas asplenii group and Pseudomonas fluorescens complex have adopted these biosynthetic strategies to co-produce their own mycin and peptin variants, in some strains supplemented with an analogue of the P. syringae linear LP (LLP), syringafactin. This capacity is not confined to phytopathogens but also occurs in some biocontrol strains, which indicates that these LP families not solely function as general virulence factors. We address this issue by scrutinizing the structural diversity and bioactivities of LPs from the mycin, peptin, and factin families in a phylogenetic and evolutionary perspective. BGC functional organization (including associated regulatory and transport genes) and NRPS modular architectures in known and candidate LP producers were assessed by genome mining.

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Section: A Plethora Of Lp-associated Luxr Regulatorsmentioning

confidence: 99%

Lipopeptide families at the interface between pathogenic and beneficialPseudomonas-plant interactions

Girard

Höfte

Mot

2020

Critical Reviews in Microbiology

106

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“…S40 also displayed antifungal activity. In order to investigate whether other biocontrol bacteria can degrade GAs, we tested the ability of the well-described antifungal strain Pseudomonas fluorescens In5 isolated from a potato field in southern Greenland ( Michelsen and Stougaard, 2011 ; Hennessy et al, 2017 ). We observed that P. fluorescens In5 was able to degrade both α-chaconine and α-solanine and similar to the GA-degraders described in this study, appeared to be capable of the complete degradation and metabolism of both compounds as no solanidine was detected following hydrolysis of the GAs by a crude enzyme extract from P. fluorescens In5.…”

Section: Resultsmentioning

confidence: 99%

A Screening Method for the Isolation of Bacteria Capable of Degrading Toxic Steroidal Glycoalkaloids Present in Potato

et al. 2018

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Potato juice, a by-product of starch processing, is a potential high-value food ingredient due to its high protein content. However, conversion from feed to human protein requires the removal of the toxic antinutritional glycoalkaloids (GAs) α-chaconine and α-solanine. Detoxification by enzymatic removal could potentially provide an effective and environmentally friendly process for potato-derived food protein production. While degradation of GAs by microorganisms has been documented, there exists limited knowledge on the enzymes involved and in particular how bacteria degrade and metabolize GAs. Here we describe a series of methods for the isolation, screening, and selection of GA-degrading bacteria. Bacterial cultures from soils surrounding greened potatoes, including the potato peels, were established and select bacterial isolates were studied. Screening of bacterial crude extracts for the ability to hydrolyze GAs was performed using a combination of thin layer chromatography (TLC), high performance liquid chromatography (HPLC), and liquid chromatography mass spectrometry (LC-MS). Analysis of the 16S rRNA sequences revealed that bacteria within the genus Arthrobacter were among the most efficient GA-degrading strains.

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“…We have previously shown that in P. fluorescens In5, NunF, a homolog to SyrF, positively regulates synthesis of both nunamycin and nunapeptin and that nunF expression was strongly upregulated in response to both carbon sources indicating the presence of a fungus (27) and during interaction with the fungus Fusarium graminearum (31). In this study, we investigate the induction pattern of In5 nunF and gacA in relation to fungal and plant signal molecules, and we show that In5 gacA is slightly upregulated by arbutin but not by fungal molecules whereas nunF is upregulated only by fungal signaling molecules but not by plant phenolics.…”

Section: Downloaded Frommentioning

confidence: 99%

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

Christiansen

Alanin

Phippen

et al. 2020

Appl Environ Microbiol

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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 signalling 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 focusses 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 signalling molecules leading to the hypothesis that P. fluorescens is a hyphosphere-associated bacterium encoding 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 structure of the peptides synthesized is 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 code 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 pathogenic P. syringae pv. syringae is induced by plant signalling molecules, such compounds do not significantly influence synthesis of nunamycin and nunapeptin in P. fluorescens In5. Instead, fungal-associated molecules positively regulate anti-fungal 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.

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Biosynthesis of the antimicrobial cyclic lipopeptides nunamycin and nunapeptin by Pseudomonas fluorescens strain In5 is regulated by the LuxR‐type transcriptional regulator NunF

Cited by 29 publications

References 63 publications

Lipopeptide families at the interface between pathogenic and beneficialPseudomonas-plant interactions

Lipopeptide families at the interface between pathogenic and beneficialPseudomonas-plant interactions

A Screening Method for the Isolation of Bacteria Capable of Degrading Toxic Steroidal Glycoalkaloids Present in Potato

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

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