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Title: Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche

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 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 expressedmore » 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.« less

Authors:
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Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1241235
Report Number(s):
LBNL-7025E
Journal ID: ISSN 0027-8424
DOE Contract Number:  
DE-AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 109; Journal Issue: 43; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; carbohydrate-active enzymes, humic substances, litter decay wood, decay fungi

Citation Formats

Morin, Emmanuelle, Kohler, Annegret, Baker, Adam R., Foulongne-Oriol, Marie, Lombard, Vincent, Nagy, Laszlo G., Ohm, Robin A., Patyshakuliyeva, Aleksandrina, Brun, Annick, Aerts, Andrea L., Bailey, Andrew M., Billette, Christophe, Coutinho, Pedro M., Deakin, Greg, Doddapaneni, Harshavardhan, Floudas, Dimitrios, Grimwood, Jane, Hilden, Kristiina, Kues, Ursula, LaButti, Kurt M., Lapidus, Alla, Lindquist, Erika A., Lucas, Susan M., Murat, Claude, Riley, Robert W., Salamov, Asaf A., Schmutz, Jeremy, Subramanian, Venkataramanan, Wosten, Han A. B., Xu, Jianping, Eastwood, Daniel C., Foster, Gary D., Sonnenberg, Anton S. M., Cullen, Dan, de Vries, Ronald P., Lundell, Taina, Hibbett, David S., Henrissat, Bernard, Burton, Kerry S., Kerrigan, Richard W., Challen, Michael P., Grigoriev, Igor V., and Martin, Francis. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. United States: N. p., 2012. Web. doi:10.1073/pnas.1206847109.
Morin, Emmanuelle, Kohler, Annegret, Baker, Adam R., Foulongne-Oriol, Marie, Lombard, Vincent, Nagy, Laszlo G., Ohm, Robin A., Patyshakuliyeva, Aleksandrina, Brun, Annick, Aerts, Andrea L., Bailey, Andrew M., Billette, Christophe, Coutinho, Pedro M., Deakin, Greg, Doddapaneni, Harshavardhan, Floudas, Dimitrios, Grimwood, Jane, Hilden, Kristiina, Kues, Ursula, LaButti, Kurt M., Lapidus, Alla, Lindquist, Erika A., Lucas, Susan M., Murat, Claude, Riley, Robert W., Salamov, Asaf A., Schmutz, Jeremy, Subramanian, Venkataramanan, Wosten, Han A. B., Xu, Jianping, Eastwood, Daniel C., Foster, Gary D., Sonnenberg, Anton S. M., Cullen, Dan, de Vries, Ronald P., Lundell, Taina, Hibbett, David S., Henrissat, Bernard, Burton, Kerry S., Kerrigan, Richard W., Challen, Michael P., Grigoriev, Igor V., & Martin, Francis. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. United States. https://doi.org/10.1073/pnas.1206847109
Morin, Emmanuelle, Kohler, Annegret, Baker, Adam R., Foulongne-Oriol, Marie, Lombard, Vincent, Nagy, Laszlo G., Ohm, Robin A., Patyshakuliyeva, Aleksandrina, Brun, Annick, Aerts, Andrea L., Bailey, Andrew M., Billette, Christophe, Coutinho, Pedro M., Deakin, Greg, Doddapaneni, Harshavardhan, Floudas, Dimitrios, Grimwood, Jane, Hilden, Kristiina, Kues, Ursula, LaButti, Kurt M., Lapidus, Alla, Lindquist, Erika A., Lucas, Susan M., Murat, Claude, Riley, Robert W., Salamov, Asaf A., Schmutz, Jeremy, Subramanian, Venkataramanan, Wosten, Han A. B., Xu, Jianping, Eastwood, Daniel C., Foster, Gary D., Sonnenberg, Anton S. M., Cullen, Dan, de Vries, Ronald P., Lundell, Taina, Hibbett, David S., Henrissat, Bernard, Burton, Kerry S., Kerrigan, Richard W., Challen, Michael P., Grigoriev, Igor V., and Martin, Francis. 2012. "Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche". United States. https://doi.org/10.1073/pnas.1206847109. https://www.osti.gov/servlets/purl/1241235.
@article{osti_1241235,
title = {Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche},
author = {Morin, Emmanuelle and Kohler, Annegret and Baker, Adam R. and Foulongne-Oriol, Marie and Lombard, Vincent and Nagy, Laszlo G. and Ohm, Robin A. and Patyshakuliyeva, Aleksandrina and Brun, Annick and Aerts, Andrea L. and Bailey, Andrew M. and Billette, Christophe and Coutinho, Pedro M. and Deakin, Greg and Doddapaneni, Harshavardhan and Floudas, Dimitrios and Grimwood, Jane and Hilden, Kristiina and Kues, Ursula and LaButti, Kurt M. and Lapidus, Alla and Lindquist, Erika A. and Lucas, Susan M. and Murat, Claude and Riley, Robert W. and Salamov, Asaf A. and Schmutz, Jeremy and Subramanian, Venkataramanan and Wosten, Han A. B. and Xu, Jianping and Eastwood, Daniel C. and Foster, Gary D. and Sonnenberg, Anton S. M. and Cullen, Dan and de Vries, Ronald P. and Lundell, Taina and Hibbett, David S. and Henrissat, Bernard and Burton, Kerry S. and Kerrigan, Richard W. and Challen, Michael P. and Grigoriev, Igor V. and Martin, Francis},
abstractNote = {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 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.},
doi = {10.1073/pnas.1206847109},
url = {https://www.osti.gov/biblio/1241235}, journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 43,
volume = 109,
place = {United States},
year = {Fri Apr 27 00:00:00 EDT 2012},
month = {Fri Apr 27 00:00:00 EDT 2012}
}