Cargando…

Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi

Lichen-forming fungi are known to produce a large number of secondary metabolites. Some metabolites are deposited in the cortical layer of the lichen thallus where they exert important ecological functions, such as UV filtering. The fact that closely related lineages of lichen-forming fungi can diff...

Descripción completa

Detalles Bibliográficos
Autores principales: Pizarro, David, Divakar, Pradeep K, Grewe, Felix, Crespo, Ana, Dal Grande, Francesco, Lumbsch, Helge Thorsten
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7643366/
https://www.ncbi.nlm.nih.gov/pubmed/33151307
http://dx.doi.org/10.1093/gbe/evaa189
_version_ 1783606265701728256
author Pizarro, David
Divakar, Pradeep K
Grewe, Felix
Crespo, Ana
Dal Grande, Francesco
Lumbsch, Helge Thorsten
author_facet Pizarro, David
Divakar, Pradeep K
Grewe, Felix
Crespo, Ana
Dal Grande, Francesco
Lumbsch, Helge Thorsten
author_sort Pizarro, David
collection PubMed
description Lichen-forming fungi are known to produce a large number of secondary metabolites. Some metabolites are deposited in the cortical layer of the lichen thallus where they exert important ecological functions, such as UV filtering. The fact that closely related lineages of lichen-forming fungi can differ in cortical chemistry suggests that natural product biosynthesis in lichens can evolve independent from phylogenetic constraints. Usnic acid is one of the major cortical pigments in lichens. Here we used a comparative genomic approach on 46 lichen-forming fungal species of the Lecanoromycetes to elucidate the biosynthetic gene content and evolution of the gene cluster putatively responsible for the biosynthesis of usnic acid. Whole-genome sequences were gathered from taxa belonging to different orders and families of Lecanoromycetes, where Parmeliaceae is the most well-represented taxon, and analyzed with a variety of genomic tools. The highest number of biosynthetic gene clusters was found in Evernia prunastri, Pannoparmelia angustata, and Parmotrema austrosinense, respectively, and lowest in Canoparmelia nairobiensis, Bulbothrix sensibilis, and Hypotrachyna scytodes. We found that all studied species producing usnic acid contain the putative usnic acid biosynthetic gene cluster, whereas the cluster was absent in all genomes of species lacking usnic acid. The absence of the gene cluster was supported by an additional unsuccessful search for ß-ketoacylsynthase, the most conserved domain of the gene cluster, in the genomes of species lacking usnic acid. The domain architecture of this PKS cluster—homologous to the already known usnic acid PKS cluster (MPAS) and CYT450 (MPAO)—varies within the studied species, whereas the gene arrangement is highly similar in closely related taxa. We hypothesize that the ancestor of these lichen-forming fungi contained the putative usnic acid producing PKS cluster and that the gene cluster was lost repeatedly during the evolution of these groups. Our study provides insight into the genomic adaptations to the evolutionary success of these lichen-forming fungal species and sets a baseline for further exploration of biosynthetic gene content and its evolutionary significance.
format Online
Article
Text
id pubmed-7643366
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-76433662020-11-10 Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi Pizarro, David Divakar, Pradeep K Grewe, Felix Crespo, Ana Dal Grande, Francesco Lumbsch, Helge Thorsten Genome Biol Evol Research Article Lichen-forming fungi are known to produce a large number of secondary metabolites. Some metabolites are deposited in the cortical layer of the lichen thallus where they exert important ecological functions, such as UV filtering. The fact that closely related lineages of lichen-forming fungi can differ in cortical chemistry suggests that natural product biosynthesis in lichens can evolve independent from phylogenetic constraints. Usnic acid is one of the major cortical pigments in lichens. Here we used a comparative genomic approach on 46 lichen-forming fungal species of the Lecanoromycetes to elucidate the biosynthetic gene content and evolution of the gene cluster putatively responsible for the biosynthesis of usnic acid. Whole-genome sequences were gathered from taxa belonging to different orders and families of Lecanoromycetes, where Parmeliaceae is the most well-represented taxon, and analyzed with a variety of genomic tools. The highest number of biosynthetic gene clusters was found in Evernia prunastri, Pannoparmelia angustata, and Parmotrema austrosinense, respectively, and lowest in Canoparmelia nairobiensis, Bulbothrix sensibilis, and Hypotrachyna scytodes. We found that all studied species producing usnic acid contain the putative usnic acid biosynthetic gene cluster, whereas the cluster was absent in all genomes of species lacking usnic acid. The absence of the gene cluster was supported by an additional unsuccessful search for ß-ketoacylsynthase, the most conserved domain of the gene cluster, in the genomes of species lacking usnic acid. The domain architecture of this PKS cluster—homologous to the already known usnic acid PKS cluster (MPAS) and CYT450 (MPAO)—varies within the studied species, whereas the gene arrangement is highly similar in closely related taxa. We hypothesize that the ancestor of these lichen-forming fungi contained the putative usnic acid producing PKS cluster and that the gene cluster was lost repeatedly during the evolution of these groups. Our study provides insight into the genomic adaptations to the evolutionary success of these lichen-forming fungal species and sets a baseline for further exploration of biosynthetic gene content and its evolutionary significance. Oxford University Press 2020-09-10 /pmc/articles/PMC7643366/ /pubmed/33151307 http://dx.doi.org/10.1093/gbe/evaa189 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Pizarro, David
Divakar, Pradeep K
Grewe, Felix
Crespo, Ana
Dal Grande, Francesco
Lumbsch, Helge Thorsten
Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi
title Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi
title_full Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi
title_fullStr Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi
title_full_unstemmed Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi
title_short Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi
title_sort genome-wide analysis of biosynthetic gene cluster reveals correlated gene loss with absence of usnic acid in lichen-forming fungi
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7643366/
https://www.ncbi.nlm.nih.gov/pubmed/33151307
http://dx.doi.org/10.1093/gbe/evaa189
work_keys_str_mv AT pizarrodavid genomewideanalysisofbiosyntheticgeneclusterrevealscorrelatedgenelosswithabsenceofusnicacidinlichenformingfungi
AT divakarpradeepk genomewideanalysisofbiosyntheticgeneclusterrevealscorrelatedgenelosswithabsenceofusnicacidinlichenformingfungi
AT grewefelix genomewideanalysisofbiosyntheticgeneclusterrevealscorrelatedgenelosswithabsenceofusnicacidinlichenformingfungi
AT crespoana genomewideanalysisofbiosyntheticgeneclusterrevealscorrelatedgenelosswithabsenceofusnicacidinlichenformingfungi
AT dalgrandefrancesco genomewideanalysisofbiosyntheticgeneclusterrevealscorrelatedgenelosswithabsenceofusnicacidinlichenformingfungi
AT lumbschhelgethorsten genomewideanalysisofbiosyntheticgeneclusterrevealscorrelatedgenelosswithabsenceofusnicacidinlichenformingfungi