Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche
Emmanuelle Morin
(1)
,
Annegret Kohler
(1)
,
Adam R. Baker
(2)
,
Marie Foulongne-Oriol
(3)
,
Julien Lombard
(4)
,
Laszlo G. Nagy
(5)
,
Robin A. Ohm
(6, 7)
,
Aleksandrina Patyshakuliyeva
(8)
,
Annick Brun-Jacob
(1)
,
Andrea L. Aerts
(6)
,
Andrew M. Bailey
(9)
,
Christophe Billette
(3)
,
Pedro M Coutinho
(4)
,
Greg Deakin
(10)
,
Harshavardhan Doddapaneni
(11)
,
Dimitrios Floudas
(5)
,
Jane Grimwood
(9)
,
Kristiina Hildén
(12)
,
Ursula Kües
(13)
,
Kurt M. Labutti
(6)
,
Alla Lapidus
(6)
,
Erika A. Lindquist
(6)
,
Susan M. Lucas
(6)
,
Claude Murat-Furminieux
(1)
,
Robert W. Riley
(6)
,
Asaf A. Salamov
(6)
,
Jeremy Schmutz
(14)
,
Venkataramanan Subramanian
(15)
,
Han A. B. Wösten
(7)
,
Jianping Xu
(16)
,
Daniel C. Eastwood
(17)
,
Gary D. Foster
(9)
,
Anton S. M. Sonnenberg
(18)
,
Dan Cullen
(19)
,
Ronald P. de Vries
(8)
,
Taina Lundell
(12)
,
David S. Hibbett
(5)
,
Bernard Henrissat
(20)
,
Kerry S. Burton
(10)
,
Richard W. Kerrigan
(21)
,
Michael P. Challen
(22)
,
Igor V. Grigoriev
(6)
,
Francis Martin
(1)
1
IAM -
Interactions Arbres-Microorganismes
2 University of Warwick [Coventry]
3 MycSA - Unité de recherche Mycologie et Sécurité des Aliments
4 AFMB - Architecture et fonction des macromolécules biologiques
5 Clark University
6 United States Department of Energy
7 Universiteit Utrecht / Utrecht University [Utrecht]
8 KNAW - Royal Netherlands Academy of Arts and Sciences
9 University of Bristol [Bristol]
10 East Malling Research
11 Department of Biology (Carver Center for Genomics)
12 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
13 Georg-August-University of Göttingen = Georg-August-Universität Göttingen
14 Hudson Alpha Institute
15 Biosciences Center, National Renewable Energy Laboratory
16 McMaster University [Hamilton, Ontario]
17 Swansea University
18 WUR - Wageningen University and Research [Wageningen]
19 Forest Products Laboratory
20 CNRS - Centre National de la Recherche Scientifique
21 Sylvan Biosciences
22 University of Oxford
2 University of Warwick [Coventry]
3 MycSA - Unité de recherche Mycologie et Sécurité des Aliments
4 AFMB - Architecture et fonction des macromolécules biologiques
5 Clark University
6 United States Department of Energy
7 Universiteit Utrecht / Utrecht University [Utrecht]
8 KNAW - Royal Netherlands Academy of Arts and Sciences
9 University of Bristol [Bristol]
10 East Malling Research
11 Department of Biology (Carver Center for Genomics)
12 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
13 Georg-August-University of Göttingen = Georg-August-Universität Göttingen
14 Hudson Alpha Institute
15 Biosciences Center, National Renewable Energy Laboratory
16 McMaster University [Hamilton, Ontario]
17 Swansea University
18 WUR - Wageningen University and Research [Wageningen]
19 Forest Products Laboratory
20 CNRS - Centre National de la Recherche Scientifique
21 Sylvan Biosciences
22 University of Oxford
Emmanuelle Morin
- Function : Author
- PersonId : 184935
- IdHAL : eamorin
- ORCID : 0000-0002-7268-972X
Annegret Kohler
- Function : Author
- PersonId : 741288
- IdHAL : annegret-kohler
- ORCID : 0000-0002-9575-9567
- IdRef : 161080588
Marie Foulongne-Oriol
- Function : Author
- PersonId : 745921
- IdHAL : marie-foulongne-oriol
- ORCID : 0000-0002-5668-5286
- IdRef : 067319149
Julien Lombard
- Function : Author
- PersonId : 773451
- IdRef : 183994108
Annick Brun-Jacob
- Function : Author
- PersonId : 1489459
- ORCID : 0000-0002-0299-2766
Kristiina Hildén
- Function : Author
- PersonId : 776735
- ORCID : 0000-0002-0126-8186
Claude Murat-Furminieux
- Function : Author
- PersonId : 740263
- IdHAL : claudemurat
- ORCID : 0000-0003-0685-7307
- IdRef : 084060603
Jianping Xu
- Function : Author
- PersonId : 776736
- ORCID : 0000-0003-2915-2780
Francis Martin
- Function : Author
- PersonId : 1203753
- ORCID : 0000-0002-4737-3715
- IdRef : 059918268
Abstract
Agaricus bisporus is the model fungus for the adaptation, persistence, and growth in the humic-rich leaf-litter environment. Aside from its ecological role, A. bisporus has been an important component of the human diet for over 200 y and worldwide cultivation of the “button mushroom” forms a multibillion dollar industry. We present two A. bisporus genomes, their gene repertoires and transcript profiles on compost and during mushroom formation. The genomes encode a full repertoire of polysaccharide-degrading enzymes similar to that of wood-decayers. Comparative transcriptomics of mycelium grown on defined medium, casing-soil, and compost revealed genes encoding enzymes involved in xylan, cellulose, pectin, and protein degradation are more highly expressed in compost. The striking expansion of heme-thiolate peroxidases and β-etherases is distinctive from Agaricomycotina wood-decayers and suggests a broad attack on decaying lignin and related metabolites found in humic acid-rich environment. Similarly, up-regulation of these genes together with a lignolytic manganese peroxidase, multiple copper radical oxidases, and cytochrome P450s is consistent with challenges posed by complex humic-rich substrates. The gene repertoire and expression of hydrolytic enzymes in A. bisporus is substantially different from the taxonomically related ectomycorrhizal symbiont Laccaria bicolor. A common promoter motif was also identified in genes very highly expressed in humic-rich substrates. These observations reveal genetic and enzymatic mechanisms governing adaptation to the humic-rich ecological niche formed during plant degradation, further defining the critical role such fungi contribute to soil structure and carbon sequestration in terrestrial ecosystems. Genome sequence will expedite mushroom breeding for improved agronomic characteristics.