Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidus

IntroductionThe ascomycete Hymenoscyphus fraxineus, originating from Asia, is currently threatening common ash (Fraxinus excelsior) in Europe, massive ascospore production from the saprotrophic phase being a key determinant of its invasiveness.MethodsTo consider whether fungal diversity and successi...

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Main Authors: Chatchai Kosawang, Isabella Børja, Maria-Luz Herrero, Nina E. Nagy, Lene R. Nielsen, Halvor Solheim, Volkmar Timmermann, Ari M. Hietala
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1154344/full
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author Chatchai Kosawang
Isabella Børja
Isabella Børja
Maria-Luz Herrero
Nina E. Nagy
Lene R. Nielsen
Halvor Solheim
Volkmar Timmermann
Ari M. Hietala
author_facet Chatchai Kosawang
Isabella Børja
Isabella Børja
Maria-Luz Herrero
Nina E. Nagy
Lene R. Nielsen
Halvor Solheim
Volkmar Timmermann
Ari M. Hietala
author_sort Chatchai Kosawang
collection DOAJ
description IntroductionThe ascomycete Hymenoscyphus fraxineus, originating from Asia, is currently threatening common ash (Fraxinus excelsior) in Europe, massive ascospore production from the saprotrophic phase being a key determinant of its invasiveness.MethodsTo consider whether fungal diversity and succession in decomposing leaf litter are affected by this invader, we used ITS-1 metabarcoding to profile changes in fungal community composition during overwintering. The subjected ash leaf petioles, collected from a diseased forest and a healthy ash stand hosting the harmless ash endophyte Hymenoscyphus albidus, were incubated in the forest floor of the diseased stand between October 2017 and June 2018 and harvested at 2–3-month intervals.ResultsTotal fungal DNA level showed a 3-fold increase during overwintering as estimated by FungiQuant qPCR. Petioles from the healthy site showed pronounced changes during overwintering; ascomycetes of the class Dothideomycetes were predominant after leaf shed, but the basidiomycete genus Mycena (class Agaricomycetes) became predominant by April, whereas H. albidus showed low prevalence. Petioles from the diseased site showed little change during overwintering; H. fraxineus was predominant, while Mycena spp. showed increased read proportion by June.DiscussionThe low species richness and evenness in petioles from the diseased site in comparison to petioles from the healthy site were obviously related to tremendous infection pressure of H. fraxineus in diseased forests. Changes in leaf litter quality, owing to accumulation of host defense phenolics in the pathogen challenged leaves, and strong saprophytic competence of H. fraxineus are other factors that probably influence fungal succession. For additional comparison, we examined fungal community structure in petioles collected in the healthy stand in August 2013 and showing H. albidus ascomata. This species was similarly predominant in these petioles as H. fraxineus was in petioles from the diseased site, suggesting that both fungi have similar suppressive effects on fungal richness in petiole/rachis segments they have secured for completion of their life cycle. However, the ability of H. fraxineus to secure the entire leaf nerve system in diseased forests, in opposite to H. albidus, impacts the general diversity and successional trajectory of fungi in decomposing ash petioles.
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spelling doaj.art-78574c11d6c144319cf4573ad36a45f72023-04-14T04:25:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11543441154344Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidusChatchai Kosawang0Isabella Børja1Isabella Børja2Maria-Luz Herrero3Nina E. Nagy4Lene R. Nielsen5Halvor Solheim6Volkmar Timmermann7Ari M. Hietala8Department of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg, DenmarkDivision of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research (NIBIO), Ås, NorwayFaculty of Environmental Sciences and Natural Resource Management (MINA), Norwegian University of Life Sciences (NMBU), Ås, NorwayDivision of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research (NIBIO), Ås, NorwayDivision of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research (NIBIO), Ås, NorwayDepartment of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg, DenmarkDivision of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research (NIBIO), Ås, NorwayDivision of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research (NIBIO), Ås, NorwayNorwegian Institute of Bioeconomy Research (NIBIO), Steinkjer, NorwayIntroductionThe ascomycete Hymenoscyphus fraxineus, originating from Asia, is currently threatening common ash (Fraxinus excelsior) in Europe, massive ascospore production from the saprotrophic phase being a key determinant of its invasiveness.MethodsTo consider whether fungal diversity and succession in decomposing leaf litter are affected by this invader, we used ITS-1 metabarcoding to profile changes in fungal community composition during overwintering. The subjected ash leaf petioles, collected from a diseased forest and a healthy ash stand hosting the harmless ash endophyte Hymenoscyphus albidus, were incubated in the forest floor of the diseased stand between October 2017 and June 2018 and harvested at 2–3-month intervals.ResultsTotal fungal DNA level showed a 3-fold increase during overwintering as estimated by FungiQuant qPCR. Petioles from the healthy site showed pronounced changes during overwintering; ascomycetes of the class Dothideomycetes were predominant after leaf shed, but the basidiomycete genus Mycena (class Agaricomycetes) became predominant by April, whereas H. albidus showed low prevalence. Petioles from the diseased site showed little change during overwintering; H. fraxineus was predominant, while Mycena spp. showed increased read proportion by June.DiscussionThe low species richness and evenness in petioles from the diseased site in comparison to petioles from the healthy site were obviously related to tremendous infection pressure of H. fraxineus in diseased forests. Changes in leaf litter quality, owing to accumulation of host defense phenolics in the pathogen challenged leaves, and strong saprophytic competence of H. fraxineus are other factors that probably influence fungal succession. For additional comparison, we examined fungal community structure in petioles collected in the healthy stand in August 2013 and showing H. albidus ascomata. This species was similarly predominant in these petioles as H. fraxineus was in petioles from the diseased site, suggesting that both fungi have similar suppressive effects on fungal richness in petiole/rachis segments they have secured for completion of their life cycle. However, the ability of H. fraxineus to secure the entire leaf nerve system in diseased forests, in opposite to H. albidus, impacts the general diversity and successional trajectory of fungi in decomposing ash petioles.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1154344/fulldecompositionfungal community dynamicsinvasive speciesHymenoscyphus fraxineusmetabarcoding
spellingShingle Chatchai Kosawang
Isabella Børja
Isabella Børja
Maria-Luz Herrero
Nina E. Nagy
Lene R. Nielsen
Halvor Solheim
Volkmar Timmermann
Ari M. Hietala
Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidus
Frontiers in Microbiology
decomposition
fungal community dynamics
invasive species
Hymenoscyphus fraxineus
metabarcoding
title Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidus
title_full Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidus
title_fullStr Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidus
title_full_unstemmed Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidus
title_short Fungal succession in decomposing ash leaves colonized by the ash dieback pathogen Hymenoscyphus fraxineus or its harmless relative Hymenoscyphus albidus
title_sort fungal succession in decomposing ash leaves colonized by the ash dieback pathogen hymenoscyphus fraxineus or its harmless relative hymenoscyphus albidus
topic decomposition
fungal community dynamics
invasive species
Hymenoscyphus fraxineus
metabarcoding
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1154344/full
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