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Linking a Gene Cluster to Atranorin, a Major Cortical Substance of Lichens, through Genetic Dereplication and Heterologous Expression

Authors
Kim, WonyongLiu, RundongWoo, SunminKang, Kyo BinPark, HyunYu, Young HyunHa, Hyung-HoOh, Seung-YoonYang, Ji HoKim, HangunYun, Sung-HwanHur, Jae-Seoun
Issue Date
5월-2021
Publisher
AMER SOC MICROBIOLOGY
Keywords
Cladonia; lichen; atranorin; polyketides; secondary metabolism
Citation
MBIO, v.12, no.3
Indexed
SCIE
SCOPUS
Journal Title
MBIO
Volume
12
Number
3
URI
https://scholar.korea.ac.kr/handle/2021.sw.korea/137423
DOI
10.1128/mBio.01111-21
ISSN
2161-2129
Abstract
The depside and depsidone series compounds of polyketide origin accumulate in the cortical or medullary layers of lichen thalli. Despite the taxonomic and ecological significance of lichen chemistry and its pharmaceutical potentials, there has been no single piece of genetic evidence linking biosynthetic genes to lichen substances. Thus, we systematically analyzed lichen polyketide synthases (PKSs) for categorization and identifica-tion of the biosynthetic gene cluster (BGC) involved in depside/depsidone production. Our in-depth analysis of the interspecies PKS diversity in the genus Cladonia and a related Antarctic lichen, Stereocaulon alpinum, identified 45 BGC families, linking lichen PKSs to 15 previously characterized PKSs in nonlichenized fungi. Among these, we identified highly syntenic BGCs found exclusively in lichens producing atranorin (a depside). Heterologous expression of the putative atranorin PKS gene (coined atr1) yielded 4-O-demethylbarbatic acid, found in many lichens as a precursor compound, indicating an intermolecular cross linking activity of Atr1 for depside formation. Subsequent introductions of tailoring enzymes into the heterologous host yielded atranorin, one of the most common cortical substances of macrolichens. Phylogenetic analysis of fungal PKS revealed that the Atr1 is in a novel PKS clade that included two conserved lichen-specific PKS families likely involved in biosynthesis of depsides and depsidones. Here, we provide a comprehensive catalog of PKS families of the genus Cladonia and functionally characterize a biosynthetic gene cluster from lichens, establishing a cornerstone for studying the genetics and chemical evolution of diverse lichen substances. IMPORTANCE Lichens play significant roles in ecosystem function and comprise about 20% of all known fungi. Polyketide-derived natural products accumulate in the cortical and medullary layers of lichen thalli, some of which play key roles in protection from biotic and abiotic stresses (e.g., herbivore attacks and UV irradiation). To date, however, no single lichen product has been linked to respective biosynthetic genes with genetic evidence. Here, we identified a gene cluster family responsible for biosynthesis of atranorin, a cortical substance found in diverse lichen species, by categorizing lichen polyketide synthase and reconstructing the atranorin biosynthetic pathway in a heterologous host. This study will help elucidate lichen secondary metabolism, harnessing the lichen's chemical diversity, hitherto obscured due to limited genetic information on lichens.
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