4.6 Article

Identification of a biosynthetic gene cluster for a red pigment cristazarin produced by a lichen-forming fungus Cladonia metacorallifera

Journal

PLOS ONE
Volume 18, Issue 6, Pages -

Publisher

PUBLIC LIBRARY SCIENCE
DOI: 10.1371/journal.pone.0287559

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Lichens are capable of producing novel bioactive metabolites, with approximately 1,000 secondary metabolites identified to date. This study focused on the biosynthetic gene clusters (BGCs) responsible for lichen secondary metabolites, specifically the BGC for cristazarin production in Cladonia metacorallifera. Transcriptome analysis revealed a non-reducing polyketide synthase (PKS) gene, crz7, highly expressed in growth media containing fructose or glucose, indicating its involvement in cristazarin biosynthesis. The conserved BGCs related to cristazarin were also found in other species, suggesting their potential for producing cristazarin. Phylogenetic analysis and neighboring gene functions provided insights into the plausible biosynthetic route for cristazarin. This study highlights the importance of transcriptome profiling in linking metabolites of interest to their biosynthetic genes in lichens.
Lichens are known to produce many novel bioactive metabolites. To date, approximately 1,000 secondary metabolites have been discovered, which are predominantly produced by the lichen mycobionts. However, despite the extensive studies on production of lichen secondary metabolites, little is known about the responsible biosynthetic gene clusters (BGCs). Here, we identified a putative BGC that is implicated in production of a red pigment, cristazarin (a naphthazarin derivative), in Cladonia metacorallifera. Previously, cristazarin was shown to be specifically induced in growth media containing fructose as a sole carbon source. Thus, we performed transcriptome analysis of C. metacorallifera growing on different carbon sources including fructose to identify the BGC for cristazarin. Among 39 polyketide synthase (PKS) genes found in the genome of C. metacorallifera, a non-reducing PKS (coined crz7) was highly expressed in growth media containing either fructose or glucose. The borders of a cristazarin gene cluster were delimited by co-expression patterns of neighboring genes of the crz7. BGCs highly conserved to the cristazarin BGC were also found in C. borealis and C. macilenta, indicating that these related species also have metabolic potentials to produce cristazarin. Phylogenetic analysis revealed that the Crz7 is sister to fungal PKSs that biosynthesize an acetylated tetrahydoxynaphthalene as a precursor of melanin pigment. Based on the phylogenetic placement of the Crz7 and putative functions of its neighboring genes, we proposed a plausible biosynthetic route for cristazarin. In this study, we identified a lichen-specific BGC that is likely involved in the biosynthesis of a naphthazarin derivative, cristazarin, and confirmed that transcriptome profiling under inducing and non-inducing conditions is an effective strategy for linking metabolites of interest to biosynthetic genes.

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