Conserved white rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus
Shingo Miyauchi
(1, 2)
,
Hayat Hage
(1)
,
Elodie Drula
(1)
,
Laurence Lesage-Meessen
(3, 1)
,
Jean-Guy Berrin
(1)
,
David Navarro
(3, 1)
,
Anne Favel
(1)
,
Delphine Chaduli
(3, 1)
,
Sacha Grisel
(1)
,
Mireille Haon
(1)
,
François Piumi
(1)
,
Anthony Levasseur
(4, 5)
,
Anne Lomascolo
(1)
,
Steven Ahrendt
(6)
,
Kerrie Barry
(6)
,
Kurt Labutti
(6)
,
Didier Chevret
(7)
,
Chris Daum
(6)
,
Jérôme J. Mariette
(8)
,
Christophe C. Klopp
(8)
,
Daniel Cullen
(9)
,
Ronald de Vries
(10, 11)
,
Allen Gathman
(12)
,
Matthieu Hainaut
(13)
,
Bernard Henrissat
(13)
,
Kristiina Hildén
(11)
,
Ursula Kues
(14)
,
Walt Lilly
(12)
,
Anna Lipzen
(15)
,
Miia Mäkelä
(11)
,
Angel Martinez
(16)
,
Melanie Morel-Rouhier
(2)
,
Emmanuelle Morin
(2)
,
Jasmyn Pangilinan
(17)
,
Arthur Ram
(18)
,
Han Wösten
(19)
,
Francisco Ruiz-Dueñas
(16)
,
Robert Riley
(15)
,
Eric Record
(1)
,
Igor Grigoriev
(20)
,
Marie-Noelle Rosso
(1)
1
BBF -
Biodiversité et Biotechnologie Fongiques
2 IAM - Interactions Arbres-Microorganismes
3 Imagine - U1163 - Imagine - Institut des maladies génétiques (IHU)
4 MEPHI - Microbes évolution phylogénie et infections
5 IHU Marseille - Institut Hospitalier Universitaire Méditerranée Infection
6 DOE - U.S. Department of Energy [Washington]
7 MICALIS - MICrobiologie de l'ALImentation au Service de la Santé
8 MIAT INRAE - Unité de Mathématiques et Informatique Appliquées de Toulouse
9 USDA Forest Service Rocky Mountain Forest and Range Experiment Station
10 WI - Westerdijk Fungal Biodiversity Institute [Utrecht]
11 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
12 MSSU - Missouri Southern State University
13 AFMB - Architecture et fonction des macromolécules biologiques
14 Department of Molecular Cell Biology [Göttingen]
15 DOE - Department of Energy / Joint Genome Institute
16 CSIC - Centro de Investigaciones Biológicas
17 DOE Joint Genome Institute [Walnut Creek]
18 Department of Molecular Microbiology and Biotechnology
19 Utrecht University [Utrecht]
20 Department of Plant Pathology & Microbiology [Riverside]
2 IAM - Interactions Arbres-Microorganismes
3 Imagine - U1163 - Imagine - Institut des maladies génétiques (IHU)
4 MEPHI - Microbes évolution phylogénie et infections
5 IHU Marseille - Institut Hospitalier Universitaire Méditerranée Infection
6 DOE - U.S. Department of Energy [Washington]
7 MICALIS - MICrobiologie de l'ALImentation au Service de la Santé
8 MIAT INRAE - Unité de Mathématiques et Informatique Appliquées de Toulouse
9 USDA Forest Service Rocky Mountain Forest and Range Experiment Station
10 WI - Westerdijk Fungal Biodiversity Institute [Utrecht]
11 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
12 MSSU - Missouri Southern State University
13 AFMB - Architecture et fonction des macromolécules biologiques
14 Department of Molecular Cell Biology [Göttingen]
15 DOE - Department of Energy / Joint Genome Institute
16 CSIC - Centro de Investigaciones Biológicas
17 DOE Joint Genome Institute [Walnut Creek]
18 Department of Molecular Microbiology and Biotechnology
19 Utrecht University [Utrecht]
20 Department of Plant Pathology & Microbiology [Riverside]
Shingo Miyauchi
- Function : Author
- PersonId : 1017688
David Navarro
- Function : Author
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- IdHAL : david-navarro
- ORCID : 0000-0002-3266-8270
Delphine Chaduli
- Function : Author
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François Piumi
- Function : Author
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Steven Ahrendt
- Function : Author
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Kerrie Barry
- Function : Author
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- ORCID : 0000-0002-8999-6785
Kurt Labutti
- Function : Author
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- ORCID : 0000-0002-5838-1972
Didier Chevret
- Function : Author
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Jérôme J. Mariette
- Function : Author
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Christophe C. Klopp
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Bernard Henrissat
- Function : Author
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Kristiina Hildén
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- ORCID : 0000-0002-0126-8186
Anna Lipzen
- Function : Author
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Melanie Morel-Rouhier
- Function : Author
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- IdHAL : melanie-morel-rouhier
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- IdRef : 094096945
Emmanuelle Morin
- Function : Author
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- IdHAL : eamorin
- ORCID : 0000-0002-7268-972X
Francisco Ruiz-Dueñas
- Function : Author
- PersonId : 801550
- ORCID : 0000-0002-9837-5665
Eric Record
- Function : Author
- PersonId : 736772
- IdHAL : eric-record
- ORCID : 0000-0002-7545-9997
- IdRef : 168826275
Igor Grigoriev
- Function : Author
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- ORCID : 0000-0002-3136-8903
- IdRef : 229928536
Marie-Noelle Rosso
- Function : Author
- PersonId : 775264
- IdHAL : marie-noelle-rosso
- ORCID : 0000-0001-8317-7220
- IdRef : 120030535
Abstract
White-rot (WR) fungi are pivotal decomposers of dead organic matter in forest ecosystems and typically use a large array of hydrolytic and oxidative enzymes to deconstruct lignocellulose. However, the extent of lignin and cellulose degradation may vary between species and wood type. Here we combined comparative genomics, transcriptomics and secretome proteomics to identify conserved enzymatic signatures at the onset of wood decaying activity within the Basidiomycota genus Pycnoporus. We observed strong conservation in the genome structures and the repertoires of protein coding genes across the four Pycnoporus species described to date, despite the species having distinct geographic distributions. We further analyzed the early response of P. cinnabarinus, P. coccineus and P. sanguineus to diverse (ligno)-cellulosic substrates. We identified a conserved set of enzymes mobilized by the three species for breaking down cellulose, hemicellulose and pectin. The co-occurrence in the exo-proteomes of H2O2 producing enzymes with H2O2 consuming enzymes was a common feature of the three species, although each enzymatic partner displayed independent transcriptional regulation. Finally, cellobiose dehydrogenase-coding genes were systematically co-regulated with at least one AA9 LPMO gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood decaying process.