Regulation of the Synthesis and Secretion of the Iron Chelator Cyclodipeptide Pulcherriminic Acid in Bacillus licheniformis

Wang, Dong; Zhan, Yangyang; Cai, Dongbo; Li, Xiaoyun; Wang, Qin; Chen, Shouwen

doi:10.1128/aem.00262-18

Cited by 46 publications

(61 citation statements)

References 47 publications

(58 reference statements)

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“…2A) (28). The respective genes, yvmC and cypX (28), are co-located on the genome with the coding regions for a transcriptional regulator (PchR) (29) and a putative membrane bound transporter YvmA (30) (Fig. 2B).…”

Section: Strains Lacking Pulcherriminic Acid Synthesis Form "Ever-expmentioning

confidence: 99%

Pulcherrimin formation controls growth arrest of theBacillus subtilisbiofilm

Arnaouteli

Matoz-Fernandez

Porter

et al. 2019

Preprint

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Significance:Understanding the processes that underpin the mechanism of biofilm formation, dispersal, and inhibition are critical to allow exploitation and to understand how microbes thrive in the environment. Here, we reveal that the formation of an extracellular iron chelate restricts the expansion of a biofilm. The countering benefit to self-restriction of growth is protection of an environmental niche. These findings highlight the complex options and outcomes that bacteria need to balance in order to modulate their local environment to maximise colonisation, and therefore survival.

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Section: Strains Lacking Pulcherriminic Acid Synthesis Form "Ever-expmentioning

confidence: 99%

Pulcherrimin formation controls growth arrest of theBacillus subtilisbiofilm

Arnaouteli

Matoz-Fernandez

Porter

et al. 2019

Preprint

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“…Pigmentless, white mutants have previously been reported after nitrosoguanidine treatment (33) and were here found to occur spontaneously among freeze-dried M. pulcherrima cells that were stored at 22 °C for several months. Since pulcherrimin has been implicated in the antagonistic activity of M. pulcherrima and Bacillus licheniformis, supposedly due to its iron immobilizing activity (30,33), we characterised pigmentless M. pulcherrima mutants with respect to their antagonistic activity against plant pathogenic fungi.…”

Section: Resultsmentioning

confidence: 99%

“…This compound represents an insoluble complex of iron and pulcherriminic acid that forms non-enzymatically in the presence of iron III (22,24,25,41,42). Pulcherrimin formation may serve as a defence against deleterious effects of high amounts of iron (reviewed by Kluyver (22)) and is thought to deprive competing microbes of iron and thus limit their growth (9,16,30,32,33). Although pulcherrimin levels and antifungal activity seem to correlate, as suggested previously (33) and shown here by quantitative competition assays with pigmentless and complemented mutants, a causal relationship between iron deprivation and antifungal activity has not been demonstrated.…”

Section: Discussionmentioning

confidence: 99%

“…However, pulcherrimin is also produced by certain bacteria such as Bacillus licheniformis, where the two genes yvmC and cypX, coding for a cyclodipeptide synthase and cytochrome P450 oxidase, respectively, are responsible for its biosynthesis (27)(28)(29). Expression of yvmC and cypX and the formation of pulcherrimin are intricately regulated by factors such as growth stage, iron availability, or environmental stress (30,31). Iron chelation by pulcherriminic acid and formation of insoluble pulcherrimin, causing iron depletion in the growth substrate, is thought to mediate antimicrobial activity of bacteria and yeasts (9,16,30,32,33).…”

Section: Introductionmentioning

confidence: 99%

“…Expression of yvmC and cypX and the formation of pulcherrimin are intricately regulated by factors such as growth stage, iron availability, or environmental stress (30,31). Iron chelation by pulcherriminic acid and formation of insoluble pulcherrimin, causing iron depletion in the growth substrate, is thought to mediate antimicrobial activity of bacteria and yeasts (9,16,30,32,33). However, alternative hypotheses to this mode of action cannot be excluded (e.g., antimicrobial activity due to precursors and independent of iron, regulatory effect on plant, fungal or bacterial responses, defense reaction against toxic iron levels) (22,33).…”

Section: Introductionmentioning

confidence: 99%

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Snf2 controls pulcherriminic acid biosynthesis and connects pigmentation and antifungal activity of the yeastMetschnikowia pulcherrima

Gore‐Lloyd

Sumann

Brachmann

et al. 2018

Preprint

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Metschnikowia pulcherrima synthesizes the red pigment pulcherrimin, from cyclodileucine (cyclo(Leu-Leu)) as a precursor, and exhibits strong antifungal activity against notorious plant pathogenic fungi such as Botrytis and Gibberella (i.e., Fusarium). This yeast therefore has great potential for biocontrol applications against fungal diseases; particularly in the phyllosphere where this species is frequently found. To elucidate the molecular basis of the antifungal activity of M. pulcherrima, we compared a wildtype strain with a spontaneously occurring, pigmentless, weakly antagonistic mutant derivative. Whole genome sequencing of the wildtype and mutant strains identified a point mutation that creates a premature stop codon in the transcriptional regulator SNF2 in the mutant strain. Complementation of the snf2 mutant strain with the wildtype SNF2 gene restored pigmentation and recovered the strong antifungal activity of M. pulcherrima against plant pathogens in vitro and on cherries. Ultra-performance liquid chromatography-high resolution heated electrospray ionization mass spectrometry (UPLC HR HESI-MS) proved the presence and structure of the pulcherrimin precursors cyclo(Leu-Leu) and pulcherriminic acid and also identified new compounds that likely represented an additional precursor and degradation products of pulcherriminic acid and/or pulcherrimin. All of these compounds were identified in the wildtype and complemented strain, but were undetectable in the pigmentless snf2 mutant strain. These results thus identify SNF2 as a regulator of antifungal activity and pulcherriminic acid biosynthesis in M. pulcherrima and provide a starting point for deciphering the molecular functions underlying the antagonistic activity of this yeast. Significance statementMetschnikowia pulcherrima is a strongly antifungal yeast and a most promising species for the control of notorious plant diseases. This multidisciplinary study on the M. pulcherrima mode of action compared a wildtype isolate with a pigmentless mutant exhibiting reduced antifungal activity. The transcriptional regulator Snf2 was identified as a "biocontrol regulator" controlling antifungal activity of M. pulcherrima via PUL gene transcription, cyclodipeptide synthesis and additional, yet uncharacterized mechanisms. The identification of cyclo(Leu-Leu), pulcherriminic acid, as well as novel precursor and degradation products of pulcherrimin, opens up new avenues for research on the metabolism and functions of pulcherrimin. Overall, this works establishes M. pulcherrima as a genetically tractable model and will benefit the development of biocontrol solutions for important plant diseases. BIOLOGICAL SCIENCES, MicrobiologyGenome sequencing & mapping of mutations Genomic DNA of the M. pulcherrima strain APC 1.2 was extracted using the Qiagen DNeasy Plant Mini Kit and sequenced on the PacBio RS II platform (performed at the Functional Genomics Center Zurich). Subsequent de novo genome assembly, polishing and resequencing were performed using PacBio SMRT Portal 2.3.0...

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Recruiting grape‐isolated antagonistic yeasts for the sustainable bio‐management of Botrytis cinerea on grapes

Oztekin,

Karbancioglu‐Guler

2024

Food and Energy Security

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Botrytis cinerea is the causative agent of grey mould disease in grapes, which was linked to significant postharvest losses. This study examined three grape‐isolated yeasts (Metschnikowia aff. fructicola, Metschnikowia pulcherrima, and Hansenispora uvarum) through in vitro and in vivo tests on detached grape berries against grey mould, as well as the elucidation of their possible mechanisms of action. The antifungal mechanism of action of yeasts was determined by the lytic enzyme activity, inhibition of spore germination, biofilm activity, iron depletion, diffusible metabolites, wound‐site colonisation, mycocin, and volatile organic compounds (VOCs) production. The highest in vitro efficacy (83.13%) was observed on M. aff. fructicola, followed by M. pulcherrima (82.10%) and H. uvarum (71.66%). Metschnikowia yeasts exhibited comparable enzyme activities, including protease, β‐1,3 glucanase, gelatinase chitinase, and cellulase, while H. uvarum had a poor enzymatic activity with chitinase and gelatinase. M. aff. fructicola showed relatively higher iron depletion activity than M. pulcherrima, while M. pulcherrima outperformed via diffusible metabolites. All yeast cultures significantly reduced spore germination by at least 86%. Overall, M. aff. fructicola exhibited the highest biocontrol activity with its iron depletion, inhibition of conidial germination, biofilm formation, VOCs, and well colonisation on grape berries. M. aff. fructicola 1‐UDM outperformed all other yeasts by significantly reducing disease incidence and lesion diameter values (93.4% and 94.3%, respectively). Remarkably, H. uvarum VOCs demonstrated potential as a biofumigant for suppressing grey mould. All yeasts are well adapted to their ecological niche to bio‐protect grapes from grey mould disease.

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Regulation of the Synthesis and Secretion of the Iron Chelator Cyclodipeptide Pulcherriminic Acid in Bacillus licheniformis

Cited by 46 publications

References 47 publications

Pulcherrimin formation controls growth arrest of theBacillus subtilisbiofilm

Pulcherrimin formation controls growth arrest of theBacillus subtilisbiofilm

Snf2 controls pulcherriminic acid biosynthesis and connects pigmentation and antifungal activity of the yeastMetschnikowia pulcherrima

Recruiting grape‐isolated antagonistic yeasts for the sustainable bio‐management of Botrytis cinerea on grapes

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