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Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis

Author(s):

Elena Fernandez-Fueyo
Francisco J. Ruiz-Dueñas
Patricia Ferreira
Dimitrios Floudas
David S. Hibbett
Paulo Canessa
Luis F. Larrondo
Tim Y. James
Daniela Seelenfreund
Sergio Lobos
Rubén Polanco
Mario Tello
Yoichi Honda
Takahito Watanabe
Takashi Watanabe
Jae San Ryu
Christian P. Kubicek
Monika Schmoll
Amber Vanden Wymelenberg
Grzegorz Sabat
Sandra Splinter BonDurant
Khajamohiddin Syed
Jagjit S. Yadav
Harshavardhan Dodapaneni
Venkataramanan Subramanian
José L. Lavin
José A. Oguiza
Gumer Perez
Antonio G. Pisabarro
Lucia Ramirez
Francisco Santoyo
Emma Master
Pedro M. Coutinho
Bernard Henrissat
Vincent Lombard
Jon Karl Magnuson
Ursula Kües
Chiaki Hori
Kiyohiko Igarashi
Masahiro Samejima
Benjamin W. Held
Kerrie W. Barry
Kurt M. LaButti
Alla Lapidus
Erika A. Lindquist
Susan M. Lucas
Robert Riley
Asaf A. Salamov
Dirk Hoffmeister
Daniel Schwenk
Yitzhak Hadar
Oded Yarden
Ronald P. de Vries
Ad Wiebenga
Jan Stenlid
Daniel Eastwood
Igor V. Grigoriev
Randy M. Berka
Robert A. Blanchette
Phil Kersten
Angel T. Martinez
Rafael Vicuna

Year:

2012

Publication type:

Scientific Journal (JRNL)

Primary Station(s):

Forest Products Laboratory

Source:

PNAS , April 3, 2012, volume 109, number 14;2012

Description

Efficient lignin depolymerization is unique to the wood decay basidiomycetes, collectively referred to as white rot fungi. Phanerochaete chrysosporium simultaneously degrades lignin and cellulose, whereas the closely related species, Ceriporiopsis subvermispora, also depolymerizes lignin but may do so with relatively little cellulose degradation. To investigate the basis for selective ligninolysis, we conducted comparative genome analysis of C. subvermispora and P. chrysosporium. Genes encoding manganese peroxidase numbered 13 and five in C. subvermispora and P. chrysosporium, respectively. In addition, the C. subvermispora genome contains at least seven genes predicted to encode laccases, whereas the P. chrysosporium genome contains none. We also observed expansion of the number of C. subvermispora desaturase-encoding genes putatively involved in lipid metabolism. Microarray-based transcriptome analysis showed substantial upregulation of several desaturase and MnP genes in wood-containing medium. MS identified MnP proteins in C. subvermispora culture filtrates, but none in P. chrysosporium cultures. These results support the importance of MnP and a lignin degradation mechanism whereby cleavage of the dominant nonphenolic structures is mediated by lipid peroxidation products. Two C. subvermispora genes were predicted to encode peroxidases structurally similar to P. chrysosporium lignin peroxidase and, following heterologous expression in Escherichia coli, the enzymes were shown to oxidize high redox potential substrates, but not Mn2+. Apart from oxidative lignin degradation, we also examined cellulolytic and hemicellulolytic systems in both fungi. In summary, the C. subvermispora genetic inventory and expression patterns exhibit increased oxidoreductase potential and diminished cellulolytic capability relative to P. chrysosporium.

Citation

Fernandez-Fueyo, Elena; Ruiz-Dueñas, Francisco J.; Ferreira, Patricia; Floudas, Dimitrios; Hibbett, David S.; Canessa, Paulo; Larrondo, Luis F.; James, Tim Y.; Seelenfreund, Daniela; Lobos, Sergio; Polanco, Rubén; Tello, Mario; Honda, Yoichi; Watanabe, Takahito; Watanabe, Takashi; Ryu, Jae San; Kubicek, Christian P.; Schmoll, Monika; Gaskell, Jill; Hammel, Kenneth E.; St. John, Franz J.; Wymelenberg, Amber Vanden; Sabat, Grzegorz; BonDurant, Sandra Splinter; Syed, Khajamohiddin; Yadav, Jagjit S.; Dodapaneni, Harshavardhan; Subramanian, Venkataramanan; Lavin,José L.; Oguiza, José A.; Perez, Gumer; Pisabarro, Antonio G.; Ramirez, Lucia; Santoyo, Francisco; Master, Emma; Coutinho, Pedro M.; Henrissat, Bernard; Lombard, Vincent; Magnuson, Jon Karl; Kües, Ursula; Hori, Chiaki; Igarashi, Kiyohiko; Samejima, Masahiro; Held, Benjamin W.; Barry, Kerrie W.; LaButti, Kurt M.; Lapidus, Alla; Lindquist, Erika A.; Lucas, Susan M.; Riley, Robert; Salamov, Asaf A.; Hoffmeister, Dirk; Schwenk, Daniel; Hadar, Yitzhak; Yarden, Oded; de Vries, Ronald P.; Wiebenga, Ad; Stenlid, Jan; Eastwood, Daniel; Grigoriev, Igor V.; Berka, Randy M.; Blanchette, Robert A.; Kersten, Phil; Martinez, Angel T.; Vicuna, Rafael; Cullen, Daniel. 2012. Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proceedings of the National Academy of Sciences. 109(14): 5458-5463.

Cited

Publication Notes

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https://www.fs.usda.gov/treesearch/pubs/41647