Tissue-specific localization of polyketide synthase and other associated genes in the lichen, Cladonia rangiferina, using laser microdissection

Elshobary, Mostafa E.; Becker, Michael G.; Kalichuk, Jenna L.; Chan, Ainsley; Belmonte, Mark F.; Piercey‐Normore, Michele D.

doi:10.1016/j.phytochem.2018.09.011

Cited by 13 publications

(12 citation statements)

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“…An oxidase and a dehydrogenase may also be involved in the synthesis of the atranorin precursor haemmatomoyl aldehyde [ 105 ]. While the biosynthetic pathway of atranorin is still unknown, CrPKS16 may be involved in the biosynthesis of the atranorin precursors [ 106 ]. Three non-reducing PKS clades can be observed close to the orsellinic acid biosynthetic gene cluster from Aspergillus nidulans FGSCA4 and grayanic acid from Cladonia grayi ( Figure 3 ).…”

Section: Discussionmentioning

confidence: 99%

Microbial Communities of Cladonia Lichens and Their Biosynthetic Gene Clusters Potentially Encoding Natural Products

et al. 2021

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Lichens have been widely used in traditional medicine, especially by indigenous communities worldwide. However, their slow growth and difficulties in the isolation of lichen symbionts and associated microbes have hindered the pharmaceutical utilisation of lichen-produced compounds. Advances in high-throughput sequencing techniques now permit detailed investigations of the complex microbial communities formed by fungi, green algae, cyanobacteria, and other bacteria within the lichen thalli. Here, we used amplicon sequencing, shotgun metagenomics, and in silico metabolomics together with compound extractions to study reindeer lichens collected from Southern Finland. Our aim was to evaluate the potential of Cladonia species as sources of novel natural products. We compared the predicted biosynthetic pathways of lichen compounds from isolated genome-sequenced lichen fungi and our environmental samples. Potential biosynthetic genes could then be further used to produce secondary metabolites in more tractable hosts. Furthermore, we detected multiple compounds by metabolite analyses, which revealed connections between the identified biosynthetic gene clusters and their products. Taken together, our results contribute to metagenomic data studies from complex lichen-symbiotic communities and provide valuable new information for use in further biochemical and pharmacological studies.

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Section: Discussionmentioning

confidence: 99%

Microbial Communities of Cladonia Lichens and Their Biosynthetic Gene Clusters Potentially Encoding Natural Products

et al. 2021

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“…Even though, PKS16 was first proposed to be involved in grayanic acid production in Cladonia grayi (CgPKS16) [18], it was later proposed to be involved in atranorin production in C. rangiferina as well [26]. In our phylogeny, these genes were placed together with several genes from other Cladonia and lichen-forming fungi (PKS16 clade, Fig.…”

Section: Resultsmentioning

confidence: 93%

“…Atranorin is the major secondary compound known in B. rubella [64] and received attention in previous studies on different lichen-forming fungi. PKS16 genes in Cladonia rangiferina [26] and PKS23 genes in four Cladonia species and Stereocaulon alpinum [29] have been proposed to be involved in atranorin biosynthesis. In the framework of our phylogenetic results including these previously identified sequences, a putative PKS23 gene involved in atranorin production could be identified in B. rubella .…”

Section: Resultsmentioning

confidence: 99%

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High diversity of type I polyketide genes in Bacidia rubella as revealed by the comparative analysis of 23 lichen fungal genomes

Gerasimova¹,

Beck

Werth³

et al. 2022

Preprint

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Fungi involved in lichen symbioses produce a large array of different secondary metabolites. The high diversity of those substances has been known for decades and are often considered characteristic for taxonomical delimitation in lichen-forming fungi. Polyketides, the most common secondary metabolites, are synthesized by the Type I Polyketide synthases (TI-PKS) comprised of different enzymatic domains. We present a phylogenetic overview of Type I PKS genes recovered from the de-novo sequenced genome of Bacidia rubella in the context of additional twenty-one fungal genomes from the largest radiation of lichen-forming Ascomycetes (Lecanoromycetes) as well as the lichen-forming Eurotiomycete, Endocarpon pusillum. Using de-novo gene prediction and functional annotation combined with a phylogenetic analysis, we provide insights into the biosynthetic potential and PKS gene diversity of lichen-forming fungi. We discuss genes predicted in the lichen-forming fungal genomes in relation to previously characterized PKS genes from other fungi and bacteria. Our results reveal a high number of biosynthetic gene clusters and their gene domain composition. PKS gene content outnumbers known secondary substances produced by the lichen-forming fungi. We were able to assign putative functions to several of those PKS genes in silico, based on similarity to already characterized genes. In particular, we identified a putative PKS23 gene of Bacidia rubella, producing the common lichen substance atranorin. However, we also found that several lichen-forming fungi still possess homologs of different biosynthetic genes without producing the corresponding substances in detectable amounts. Although many PKSs remain without functional assignments in our analysis, our findings highlight that genes from lichen-forming fungi represent an untapped source of novel polyketide compounds. However, additional experimental approaches are necessary to link biosynthetic genes and secondary metabolites with confidence.

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“…Ascribing specific biosynthetic genes to lichen metabolites has been slow, due to a paucity of genetic information and lack of molecular tools for manipulating LFF recalcitrant to genetic transformation. To circumvent these issues, positive correlations between expression levels of biosynthetic genes and production of metabolites of interest have been used as circumstantial evidence for linking biosynthetic genes to lichen metabolites [45][46][47].…”

Section: Discussionmentioning

confidence: 99%

Transcriptome Analysis Identifies a Gene Cluster for the Biosynthesis of Biruloquinone, a Rare Phenanthraquinone, in a Lichen-Forming Fungus Cladonia macilenta

Kim

Jeong

Yun

et al. 2021

JoF

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Lichens are prolific producers of natural products of polyketide origin. We previously described a culture of lichen-forming fungus (LFF) Cladonia macilenta that produces biruloquinone, a purple pigment that is a phenanthraquinone rarely found in nature. However, there was no genetic information on the biosynthesis of biruloquinone. To identify a biosynthetic gene cluster for biruloquinone, we mined polyketide synthase (PKS) genes from the genome sequence of a LFF isolated from thalli of C. macilenta. The 38 PKS in C. macilenta are highly diverse, many of which form phylogenetic clades with PKS previously characterized in non-lichenized fungi. We compared transcriptional profiles of the 38 PKS genes in two chemotypic variants, one producing biruloquinone and the other producing no appreciable metabolite in vitro. We identified a PKS gene (hereafter PKS21) that was highly upregulated in the LFF that produces biruloquinone. The boundaries of a putative biruloquinone gene cluster were demarcated by co-expression patterns of six clustered genes, including the PKS21. Biruloquinone gene clusters exhibited a high degree of synteny between related species. In this study we identified a novel PKS family responsible for the biosynthesis of biruloquinone through whole-transcriptome analysis.

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Tissue-specific localization of polyketide synthase and other associated genes in the lichen, Cladonia rangiferina, using laser microdissection

Cited by 13 publications

References 53 publications

Microbial Communities of Cladonia Lichens and Their Biosynthetic Gene Clusters Potentially Encoding Natural Products

Microbial Communities of Cladonia Lichens and Their Biosynthetic Gene Clusters Potentially Encoding Natural Products

High diversity of type I polyketide genes in Bacidia rubella as revealed by the comparative analysis of 23 lichen fungal genomes

Transcriptome Analysis Identifies a Gene Cluster for the Biosynthesis of Biruloquinone, a Rare Phenanthraquinone, in a Lichen-Forming Fungus Cladonia macilenta

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