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CRISPR-Mediated Activation of Biosynthetic Gene Clusters for Bioactive Molecule Discovery in Filamentous Fungi

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    Research Article

    CRISPR-Mediated Activation of Biosynthetic Gene Clusters for Bioactive Molecule Discovery in Filamentous Fungi
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    • Indra Roux
      Indra Roux
      School of Molecular Sciences, University of Western Australia, Perth, WA 6009, Australia
      More by Indra Roux
    • Clara Woodcraft
      Clara Woodcraft
      School of Molecular Sciences, University of Western Australia, Perth, WA 6009, Australia
      More by Clara Woodcraft
    • Jinyu Hu
      Jinyu Hu
      School of Molecular Sciences, University of Western Australia, Perth, WA 6009, Australia
      More by Jinyu Hu
    • Rebecca Wolters
      Rebecca Wolters
      School of Molecular Sciences, University of Western Australia, Perth, WA 6009, Australia
      More by Rebecca Wolters
    • Cameron L. M. Gilchrist
      Cameron L. M. Gilchrist
      School of Molecular Sciences, University of Western Australia, Perth, WA 6009, Australia
      More by Cameron L. M. Gilchrist
    • Yit-Heng Chooi*
      Yit-Heng Chooi
      School of Molecular Sciences, University of Western Australia, Perth, WA 6009, Australia
      *Email: [email protected]
      More by Yit-Heng Chooi
      Orcidhttp://orcid.org/0000-0001-7719-7524
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    ACS Synthetic Biology

    Cite this: ACS Synth. Biol. 2020, 9, 7, 1843–1854
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    https://doi.org/10.1021/acssynbio.0c00197
    Published June 11, 2020
    Copyright © 2020 American Chemical Society
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    Abstract

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    Accessing the full biosynthetic potential encoded in the genomes of fungi is limited by the low expression of most biosynthetic gene clusters (BGCs) under common laboratory culture conditions. CRISPR-mediated transcriptional activation (CRISPRa) of fungal BGCs could accelerate genomics-driven bioactive secondary metabolite discovery. In this work, we established the first CRISPRa system for filamentous fungi. First, we constructed a CRISPR/dLbCas12a-VPR-based system and demonstrated the activation of a fluorescent reporter in Aspergillus nidulans. Then, we targeted the native nonribosomal peptide synthetase-like (NRPS-like) gene micA in both chromosomal and episomal contexts, achieving increased production of the compound microperfuranone. Finally, multigene CRISPRa led to the discovery of the mic cluster product as dehydromicroperfuranone. Additionally, we demonstrated the utility of the variant dLbCas12aD156R-VPR for CRISPRa at room temperature culture conditions. Different aspects that influence the efficiency of CRISPRa in fungi were investigated, providing a framework for the further development of fungal artificial transcription factors based on CRISPR/Cas.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acssynbio.0c00197.

    • Figures S1–S20. Fluorescence microscopy images with biological replicates, bioinformatic analysis of Aspergillus nidulans 5′ UTR features and PAM site frequency, quantification of additional micA CRISPRa assays, complete chromatograms of multiple gene activation of mic cluster with quantification, dehydromicroperfuranone isolation chromatograms, dehydromicroperfuranone NMR spectra, Cas12a protein alignment, microperfuranone standard curve and NMR spectra, overview of one-step cloning of Cas12a crRNA; Note S1 with sequence of crRNA/sgRNA expression cassettes cloning sites; Tables S1–S3 containing NMR and LC/MS-MS analysis summary (PDF)

    • Additional Tables S4–S9: Strains used in this study, vectors used in this study, protospacers targeted, oligonucleotides used to create crRNA/sgRNA, oligonucleotides, statistical analysis (XLSX)

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    ACS Synthetic Biology

    Cite this: ACS Synth. Biol. 2020, 9, 7, 1843–1854
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acssynbio.0c00197
    Published June 11, 2020
    Copyright © 2020 American Chemical Society
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