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. 2023 Oct 19;11(10):2590.
doi: 10.3390/microorganisms11102590.

Genome-Wide Analysis of the Cytochrome P450 Monooxygenases in the Lichenized Fungi of the Class Lecanoromycetes

Gugulethu Mlambo  1 , Tiara Padayachee  1 , David R Nelson  2 , Khajamohiddin Syed  1
Affiliations

Genome-Wide Analysis of the Cytochrome P450 Monooxygenases in the Lichenized Fungi of the Class Lecanoromycetes

Gugulethu Mlambo et al. Microorganisms. .

Abstract

Lichens are unique organisms that exhibit a permanent symbiosis between fungi and algae or fungi and photosynthetic bacteria. Lichens have been found to produce biotechnologically valuable secondary metabolites. A handful of studies showed that tailoring enzymes such as cytochrome P450 monooxygenases (CYPs/P450s) play a key role in synthesizing these metabolites. Despite the critical role of P450s in the biosynthesis of secondary metabolites, the systematic analysis of P450s in lichens has yet to be reported. This study is aimed to address this research gap. A genome-wide analysis of P450s in five lichens from the fungal class Lecanoromycetes revealed the presence of 434 P450s that are grouped into 178 P450 families and 345 P450 subfamilies. The study indicated that none of the P450 families bloomed, and 15 P450 families were conserved in all five Lecanoromycetes. Lecanoromycetes have more P450s and higher P450 family diversity compared to Pezizomycetes. A total of 73 P450s were found to be part of secondary metabolite gene clusters, indicating their potential involvement in the biosynthesis of secondary metabolites. Annotation of P450s revealed that CYP682BG1 and CYP682BG2 from Cladonia grayi and Pseudevernia furfuracea (physodic acid chemotype) are involved in the synthesis of grayanic acid and physodic acid, CYP65FQ2 from Stereocaulon alpinum is involved in the synthesis of atranorin, and CYP6309A2 from Cladonia uncialis is involved in the synthesis of usnic acid. This study serves as a reference for future annotation of P450s in lichens.

Keywords: CYPs; Lecanoromycetes; P450s; Pezizomycetes; biosynthetic gene clusters; depside; depsidone; genome-wide data-mining; lichens; phylogenetic analysis.

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Conflict of interest statement

The authors declare no conflict of interest and the funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Figures

Figure 1
Figure 1
Analysis of P450s in the five Lecanoromycetes. Identification of P450s (A) and species level comparison of P450s (B) in the five Lecanoromycetes. Species codes: Grascr1, Graphis scripta CBS 132367; Dibbae1, Dibaeis baeomyces; Clagr3, Cladonia grayi Cgr/DA2myc/ss; Acastr1, Acarospora Strigata CBS 132363; Umbpus1, Umbilicaria pustulata.
Figure 2
Figure 2
Phylogenetic analysis of Lecanoromycetes P450s. A single P450 from each of the 178 P450 families was used to construct the tree, except for P450 families with ten or more members highlighted in different colors; all members were included, and the branch collapsed. A high-quality figure with all 434 P450s is presented in Supplementary Figure S1.
Figure 3
Figure 3
Comparative analysis of P450s, P450 families, and P450 subfamilies in five the Lecanoromycetes. Detailed information is presented in Table S1. Species codes: Grascr1, Graphis scripta CBS 132367; Dibbae1, Dibaeis baeomyces; Clagr3, Cladonia grayi Cgr/DA2myc/ss; Acastr1, Acarospora Strigata CBS 132363; Umbpus1, Umbilicaria pustulata.
Figure 4
Figure 4
Comparative analysis of P450 families between Lecanoromycetes and Pezizomycetes. The number indicates the total number of P450 families.
Figure 5
Figure 5
Analysis of P450 family conservation in the five Lecanoromycetes. P450 families that are conserved in three or more species are presented. The heat map shows that the P450 family is either present (red) or absent (green) in Lecanoromycetes. The horizontal axis is made up of P450 families, and the vertical axis is made up of Lecanoromycetes. Table S2 provides a thorough examination of P450 family conservation in Lecanoromycetes.
Figure 6
Figure 6
Role of lichen P450s in the biosynthesis of different secondary metabolites. (A,B) Conversion of depside to depsidone by CYP682BG1 and CYP682BG2. (C) Oxidation of 4-O-demethylbarbatic acid and proatranorin I by CYP65Q2. (D) Oxidative dimerization of methylphloracetophenone to usnic acid by CYP6309A2.
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