Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>

The coprophilous ascomycete <i>Podospora anserina</i> is known to have a high potential to synthesize a wide array of secondary metabolites (SMs). However, to date, the characterization of SMs in this species, as in other filamentous fungal species, is far less than expected by the funct...

Full description

Bibliographic Details
Main Authors: Ling Shen, Catherine Roullier, François-Hugues Porée, Thomas Gaslonde, Ludivine Riffault-Valois, Olivier Grovel, Gwenaël Ruprich-Robert, Florence Chapeland-Leclerc
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/9/1/9
_version_ 1797440300262621184
author Ling Shen
Catherine Roullier
François-Hugues Porée
Thomas Gaslonde
Ludivine Riffault-Valois
Olivier Grovel
Gwenaël Ruprich-Robert
Florence Chapeland-Leclerc
author_facet Ling Shen
Catherine Roullier
François-Hugues Porée
Thomas Gaslonde
Ludivine Riffault-Valois
Olivier Grovel
Gwenaël Ruprich-Robert
Florence Chapeland-Leclerc
author_sort Ling Shen
collection DOAJ
description The coprophilous ascomycete <i>Podospora anserina</i> is known to have a high potential to synthesize a wide array of secondary metabolites (SMs). However, to date, the characterization of SMs in this species, as in other filamentous fungal species, is far less than expected by the functional prediction through genome mining, likely due to the inactivity of most SMs biosynthesis gene clusters (BGCs) under standard conditions. In this work, our main objective was to compare the global strategies usually used to deregulate SM gene clusters in <i>P. anserina</i>, including the variation of culture conditions and the modification of the chromatin state either by genetic manipulation or by chemical treatment, and to show the complementarity of the approaches between them. In this way, we showed that the metabolomics-driven comparative analysis unveils the unexpected diversity of metabolic changes in <i>P. anserina</i> and that the integrated strategies have a mutual complementary effect on the expression of the fungal metabolome. Then, our results demonstrate that metabolite production is significantly influenced by varied cultivation states and epigenetic modifications. We believe that the strategy described in this study will facilitate the discovery of fungal metabolites of interest and will improve the ability to prioritize the production of specific fungal SMs with an optimized treatment.
first_indexed 2024-03-09T12:05:13Z
format Article
id doaj.art-edef326360094626bd0098865a2d1908
institution Directory Open Access Journal
issn 2309-608X
language English
last_indexed 2024-03-09T12:05:13Z
publishDate 2022-12-01
publisher MDPI AG
record_format Article
series Journal of Fungi
spelling doaj.art-edef326360094626bd0098865a2d19082023-11-30T22:59:06ZengMDPI AGJournal of Fungi2309-608X2022-12-0191910.3390/jof9010009Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>Ling Shen0Catherine Roullier1François-Hugues Porée2Thomas Gaslonde3Ludivine Riffault-Valois4Olivier Grovel5Gwenaël Ruprich-Robert6Florence Chapeland-Leclerc7School of Life Science, Jiangsu Normal University, Xuzhou 221116, ChinaInstitut des Substances et Organismes de la Mer (ISOMER), UR 2160, Nantes Université, F-44000 Nantes, FranceLaboratoire de Chimie Thérapeutique, UMR 6226, ISCR, CNRS, Faculté de Pharmacie, Université de Rennes 1, F-35065 Rennes, FranceCibles Thérapeutiques et Conception de Médicaments (CiTCoM), UMR 8038, CNRS, Faculté de Pharmacie de Paris, Université Paris Cité, F-75006 Paris, FranceInstitut Pluridisciplinaire Hubert Curien, UMR 7178, CNRS, Université de Strasbourg, F-67000 Strasbourg, FranceInstitut des Substances et Organismes de la Mer (ISOMER), UR 2160, Nantes Université, F-44000 Nantes, FranceLaboratoire Interdisciplinaire des Energies de Demain (LIED), UMR 8236, CNRS, Université Paris Cité, F-75013 Paris, FranceLaboratoire Interdisciplinaire des Energies de Demain (LIED), UMR 8236, CNRS, Université Paris Cité, F-75013 Paris, FranceThe coprophilous ascomycete <i>Podospora anserina</i> is known to have a high potential to synthesize a wide array of secondary metabolites (SMs). However, to date, the characterization of SMs in this species, as in other filamentous fungal species, is far less than expected by the functional prediction through genome mining, likely due to the inactivity of most SMs biosynthesis gene clusters (BGCs) under standard conditions. In this work, our main objective was to compare the global strategies usually used to deregulate SM gene clusters in <i>P. anserina</i>, including the variation of culture conditions and the modification of the chromatin state either by genetic manipulation or by chemical treatment, and to show the complementarity of the approaches between them. In this way, we showed that the metabolomics-driven comparative analysis unveils the unexpected diversity of metabolic changes in <i>P. anserina</i> and that the integrated strategies have a mutual complementary effect on the expression of the fungal metabolome. Then, our results demonstrate that metabolite production is significantly influenced by varied cultivation states and epigenetic modifications. We believe that the strategy described in this study will facilitate the discovery of fungal metabolites of interest and will improve the ability to prioritize the production of specific fungal SMs with an optimized treatment.https://www.mdpi.com/2309-608X/9/1/9<i>Podospora anserina</i>secondary metabolitescomplementary strategiesmetabolomics
spellingShingle Ling Shen
Catherine Roullier
François-Hugues Porée
Thomas Gaslonde
Ludivine Riffault-Valois
Olivier Grovel
Gwenaël Ruprich-Robert
Florence Chapeland-Leclerc
Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>
Journal of Fungi
<i>Podospora anserina</i>
secondary metabolites
complementary strategies
metabolomics
title Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>
title_full Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>
title_fullStr Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>
title_full_unstemmed Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>
title_short Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus <i>Podospora anserina</i>
title_sort complementary strategies to unlock biosynthesis gene clusters encoding secondary metabolites in the filamentous fungus i podospora anserina i
topic <i>Podospora anserina</i>
secondary metabolites
complementary strategies
metabolomics
url https://www.mdpi.com/2309-608X/9/1/9
work_keys_str_mv AT lingshen complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai
AT catherineroullier complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai
AT francoishuguesporee complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai
AT thomasgaslonde complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai
AT ludivineriffaultvalois complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai
AT oliviergrovel complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai
AT gwenaelruprichrobert complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai
AT florencechapelandleclerc complementarystrategiestounlockbiosynthesisgeneclustersencodingsecondarymetabolitesinthefilamentousfungusipodosporaanserinai