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

E. Fernandez-Fueyo; F.J. Ruiz-Duenas; P. Ferreira; D. Floudas; D.S. Hibbett; P. Canessa; L.F. Larrondo; T.Y. James; D. Seelenfreund; S. Lobos; R. Polanco; M. Tello; Y. Honda; T. Watanabe; J.S. Ryu; C.P. Kubicek; M. Schmoll; J. Gaskell; K.E. Hammel; F.J. St John; A. Vanden Wymelenberg; G. Sabat; S. Splinter BonDurant; K. Syed; J.S. Yadav; H. Doddapaneni; V. Subramanian; J.L. Lavin; J.A. Oguiza; G. Perez; A.G. Pisabarro; L. Ramirez; F. Santoyo; E. Master; P.M. Coutinho; B. Henrissat; V. Lombard; J.K. Magnuson; U. Kues; C. Hori; K. Igarashi; M. Samejima; B.W. Held; K.W. Barry; K.M. LaButti; A. Lapidus; E.A. Lindquist; S.M. Lucas; R. Riley; A.A. Salamov; D. Hoffmeister; D. Schwenk; Y. Hadar; O. Yarden; R.P. de Vries; A. Wiebenga; J. Stenlid; D. Eastwood; I.V. Grigoriev; R.M. Berka; R.A. Blanchette; P. Kersten; A.T. Martinez; R. Vicuna; D. Cullen

doi:10.1073/pnas.1119912109

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

E. Fernandez-Fueyo, F.J. Ruiz-Duenas, P. Ferreira, D. Floudas, D.S. Hibbett, P. Canessa, L.F. Larrondo, T.Y. James, D. Seelenfreund, S. Lobos, R. Polanco, M. Tello, Y. Honda, T. Watanabe, J.S. Ryu, C.P. Kubicek, M. Schmoll, J. Gaskell, K.E. Hammel, F.J. St JohnA. Vanden Wymelenberg, G. Sabat, S. Splinter BonDurant, K. Syed, J.S. Yadav, H. Doddapaneni, V. Subramanian, J.L. Lavin, J.A. Oguiza, G. Perez, A.G. Pisabarro, L. Ramirez, F. Santoyo, E. Master, P.M. Coutinho, B. Henrissat, V. Lombard, J.K. Magnuson, U. Kues, C. Hori, K. Igarashi, M. Samejima, B.W. Held, K.W. Barry, K.M. LaButti, A. Lapidus, E.A. Lindquist, S.M. Lucas, R. Riley, A.A. Salamov, D. Hoffmeister, D. Schwenk, Y. Hadar, O. Yarden, R.P. de Vries, A. Wiebenga, J. Stenlid, D. Eastwood, I.V. Grigoriev, R.M. Berka, R.A. Blanchette, P. Kersten, A.T. Martinez, R. Vicuna, D. Cullen

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

230 Citations (Scopus)

Abstract

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 up-regulation 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.

Original language	English
Pages (from-to)	5458-5463
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	109
Issue number	14
DOIs	https://doi.org/10.1073/pnas.1119912109
Publication status	Published - 2012

Access to Document

10.1073/pnas.1119912109

Cite this

Fernandez-Fueyo, E., Ruiz-Duenas, F. J., Ferreira, P., Floudas, D., Hibbett, D. S., Canessa, P., Larrondo, L. F., James, T. Y., Seelenfreund, D., Lobos, S., Polanco, R., Tello, M., Honda, Y., Watanabe, T., Ryu, J. S., Kubicek, C. P., Schmoll, M., Gaskell, J., Hammel, K. E., ... Cullen, D. (2012). Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proceedings of the National Academy of Sciences of the United States of America, 109(14), 5458-5463. https://doi.org/10.1073/pnas.1119912109

@article{9702025db047483dbeaccb90c71b5795,

title = "Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis",

abstract = "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 up-regulation 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.",

author = "E. Fernandez-Fueyo and F.J. Ruiz-Duenas and P. Ferreira and D. Floudas and D.S. Hibbett and P. Canessa and L.F. Larrondo and T.Y. James and D. Seelenfreund and S. Lobos and R. Polanco and M. Tello and Y. Honda and T. Watanabe and J.S. Ryu and C.P. Kubicek and M. Schmoll and J. Gaskell and K.E. Hammel and {St John}, F.J. and {Vanden Wymelenberg}, A. and G. Sabat and {Splinter BonDurant}, S. and K. Syed and J.S. Yadav and H. Doddapaneni and V. Subramanian and J.L. Lavin and J.A. Oguiza and G. Perez and A.G. Pisabarro and L. Ramirez and F. Santoyo and E. Master and P.M. Coutinho and B. Henrissat and V. Lombard and J.K. Magnuson and U. Kues and C. Hori and K. Igarashi and M. Samejima and B.W. Held and K.W. Barry and K.M. LaButti and A. Lapidus and E.A. Lindquist and S.M. Lucas and R. Riley and A.A. Salamov and D. Hoffmeister and D. Schwenk and Y. Hadar and O. Yarden and {de Vries}, R.P. and A. Wiebenga and J. Stenlid and D. Eastwood and I.V. Grigoriev and R.M. Berka and R.A. Blanchette and P. Kersten and A.T. Martinez and R. Vicuna and D. Cullen",

note = "Reporting year: 2012 Metis note: 3325662",

year = "2012",

doi = "10.1073/pnas.1119912109",

language = "English",

volume = "109",

pages = "5458--5463",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "14",

}

Fernandez-Fueyo, E, Ruiz-Duenas, FJ, Ferreira, P, Floudas, D, Hibbett, DS, Canessa, P, Larrondo, LF, James, TY, Seelenfreund, D, Lobos, S, Polanco, R, Tello, M, Honda, Y, Watanabe, T, Ryu, JS, Kubicek, CP, Schmoll, M, Gaskell, J, Hammel, KE, St John, FJ, Vanden Wymelenberg, A, Sabat, G, Splinter BonDurant, S, Syed, K, Yadav, JS, Doddapaneni, H, Subramanian, V, Lavin, JL, Oguiza, JA, Perez, G, Pisabarro, AG, Ramirez, L, Santoyo, F, Master, E, Coutinho, PM, Henrissat, B, Lombard, V, Magnuson, JK, Kues, U, Hori, C, Igarashi, K, Samejima, M, Held, BW, Barry, KW, LaButti, KM, Lapidus, A, Lindquist, EA, Lucas, SM, Riley, R, Salamov, AA, Hoffmeister, D, Schwenk, D, Hadar, Y, Yarden, O, de Vries, RP, Wiebenga, A, Stenlid, J, Eastwood, D, Grigoriev, IV, Berka, RM, Blanchette, RA, Kersten, P, Martinez, AT, Vicuna, R & Cullen, D 2012, 'Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis', Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 14, pp. 5458-5463. https://doi.org/10.1073/pnas.1119912109

Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. / Fernandez-Fueyo, E.; Ruiz-Duenas, F.J.; Ferreira, P. et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 14, 2012, p. 5458-5463.

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

TY - JOUR

T1 - Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis

AU - Fernandez-Fueyo, E.

AU - Ruiz-Duenas, F.J.

AU - Ferreira, P.

AU - Floudas, D.

AU - Hibbett, D.S.

AU - Canessa, P.

AU - Larrondo, L.F.

AU - James, T.Y.

AU - Seelenfreund, D.

AU - Lobos, S.

AU - Polanco, R.

AU - Tello, M.

AU - Honda, Y.

AU - Watanabe, T.

AU - Ryu, J.S.

AU - Kubicek, C.P.

AU - Schmoll, M.

AU - Gaskell, J.

AU - Hammel, K.E.

AU - St John, F.J.

AU - Vanden Wymelenberg, A.

AU - Sabat, G.

AU - Splinter BonDurant, S.

AU - Syed, K.

AU - Yadav, J.S.

AU - Doddapaneni, H.

AU - Subramanian, V.

AU - Lavin, J.L.

AU - Oguiza, J.A.

AU - Perez, G.

AU - Pisabarro, A.G.

AU - Ramirez, L.

AU - Santoyo, F.

AU - Master, E.

AU - Coutinho, P.M.

AU - Henrissat, B.

AU - Lombard, V.

AU - Magnuson, J.K.

AU - Kues, U.

AU - Hori, C.

AU - Igarashi, K.

AU - Samejima, M.

AU - Held, B.W.

AU - Barry, K.W.

AU - LaButti, K.M.

AU - Lapidus, A.

AU - Lindquist, E.A.

AU - Lucas, S.M.

AU - Riley, R.

AU - Salamov, A.A.

AU - Hoffmeister, D.

AU - Schwenk, D.

AU - Hadar, Y.

AU - Yarden, O.

AU - de Vries, R.P.

AU - Wiebenga, A.

AU - Stenlid, J.

AU - Eastwood, D.

AU - Grigoriev, I.V.

AU - Berka, R.M.

AU - Blanchette, R.A.

AU - Kersten, P.

AU - Martinez, A.T.

AU - Vicuna, R.

AU - Cullen, D.

N1 - Reporting year: 2012 Metis note: 3325662

PY - 2012

Y1 - 2012

N2 - 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 up-regulation 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.

AB - 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 up-regulation 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.

U2 - 10.1073/pnas.1119912109

DO - 10.1073/pnas.1119912109

M3 - Article

SN - 0027-8424

VL - 109

SP - 5458

EP - 5463

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 14

ER -

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

Abstract

Access to Document

Fingerprint

Cite this