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

Deborah Gore-Lloyd, Inés Sumann, Alexander O. Brachmann, Kerstin Schneeberger, Raúl A. Ortiz-Merino, Mauro Moreno-Beltrán, Michael Schläfli, Pascal Kirner, Amanda Santos Kron, Kenneth H. Wolfe, Jörn Piel, Christian H. Ahrens, Daniel Henk, View ORCID ProfileFlorian M. Freimoser
doi: https://doi.org/10.1101/494922
Deborah Gore-Lloyd
1Department of Biology & Biochemistry, University of Bath, Bath, BA2 7AY, UK
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Inés Sumann
2Agroscope, Research Division Plant Protection, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland
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Alexander O. Brachmann
3Institute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zürich, 8093 Zürich, Switzerland
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Kerstin Schneeberger
4Agroscope, Competence Division Method Development and Analytics, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland
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Raúl A. Ortiz-Merino
5Conway Institute, University College Dublin, Dublin 4, Ireland
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Mauro Moreno-Beltrán
1Department of Biology & Biochemistry, University of Bath, Bath, BA2 7AY, UK
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Michael Schläfli
2Agroscope, Research Division Plant Protection, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland
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Pascal Kirner
2Agroscope, Research Division Plant Protection, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland
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Amanda Santos Kron
2Agroscope, Research Division Plant Protection, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland
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Kenneth H. Wolfe
5Conway Institute, University College Dublin, Dublin 4, Ireland
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Jörn Piel
3Institute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zürich, 8093 Zürich, Switzerland
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Christian H. Ahrens
4Agroscope, Competence Division Method Development and Analytics, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland
6SIB, Swiss Institute of Bioinformatics, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland.
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Daniel Henk
1Department of Biology & Biochemistry, University of Bath, Bath, BA2 7AY, UK
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Florian M. Freimoser
2Agroscope, Research Division Plant Protection, Müller-Thurgau-Strasse 29, 8820 Wädenswil, Switzerland
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  • ORCID record for Florian M. Freimoser
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Abstract

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 statement Metschnikowia 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.

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Posted December 13, 2018.
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Snf2 controls pulcherriminic acid biosynthesis and connects pigmentation and antifungal activity of the yeast Metschnikowia pulcherrima
Deborah Gore-Lloyd, Inés Sumann, Alexander O. Brachmann, Kerstin Schneeberger, Raúl A. Ortiz-Merino, Mauro Moreno-Beltrán, Michael Schläfli, Pascal Kirner, Amanda Santos Kron, Kenneth H. Wolfe, Jörn Piel, Christian H. Ahrens, Daniel Henk, Florian M. Freimoser
bioRxiv 494922; doi: https://doi.org/10.1101/494922
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Snf2 controls pulcherriminic acid biosynthesis and connects pigmentation and antifungal activity of the yeast Metschnikowia pulcherrima
Deborah Gore-Lloyd, Inés Sumann, Alexander O. Brachmann, Kerstin Schneeberger, Raúl A. Ortiz-Merino, Mauro Moreno-Beltrán, Michael Schläfli, Pascal Kirner, Amanda Santos Kron, Kenneth H. Wolfe, Jörn Piel, Christian H. Ahrens, Daniel Henk, Florian M. Freimoser
bioRxiv 494922; doi: https://doi.org/10.1101/494922

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