A fungal family of lytic polysaccharide monooxygenase-like copper proteins

Paul Howard Walton; Aurore Labourel; Kristian E H Frandsen; Feng Zhang; Nicolas Brouilly; Sacha Grisel; Mireille Haon; Luisa Ciano; David Ropartz; Mathieu Fanuel; Francis Martin; David Navarro; Marie-Noëlle Rosso; Tobias Tandrup; Bastien Bissaro; Katja Johansen; Anastasia Zerva; Bernard Henrissat; Leila Lo Leggio; Jean-Guy Berrin

doi:10.1038/s41589-019-0438-8

A fungal family of lytic polysaccharide monooxygenase-like copper proteins

Paul Howard Walton, Aurore Labourel, Kristian E H Frandsen, Feng Zhang, Nicolas Brouilly, Sacha Grisel, Mireille Haon, Luisa Ciano, David Ropartz, Mathieu Fanuel, Francis Martin, David Navarro, Marie-Noëlle Rosso, Tobias Tandrup, Bastien Bissaro, Katja Johansen, Anastasia Zerva, Bernard Henrissat, Leila Lo Leggio, Jean-Guy Berrin

Chemistry

Research output: Contribution to journal › Article › peer-review

Abstract

Lytic polysaccharide monooxygenases (LPMOs) are copper-containing enzymes that play a key role in the oxidative degradation of various biopolymers such as cellulose and chitin. While hunting for new LPMOs, we identified a new family of proteins, defined here as X325, in various fungal lineages. The three-dimensional structure of X325 revealed an overall LPMO fold and a His brace with an additional Asp ligand to Cu(II). Although LPMO-type activity of X325 members was initially expected, we demonstrated that X325 members do not perform oxidative cleavage of polysaccharides, establishing that X325s are not LPMOs. Investigations of the biological role of X325 in the ectomycorrhizal fungus Laccaria bicolor revealed exposure of the X325 protein at the interface between fungal hyphae and tree rootlet cells. Our results provide insights into a family of copper-containing proteins, which is widespread in the fungal kingdom and is evolutionarily related to LPMOs, but has diverged to biological functions other than polysaccharide degradation.

Original language	English
Article number	https://doi.org/10.1038/s41589-019-0438-8
Pages (from-to)	1-11
Number of pages	11
Journal	NATURE CHEMICAL BIOLOGY
DOIs	https://doi.org/10.1038/s41589-019-0438-8
Publication status	Published - 13 Jan 2020

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© 2020 Springer Nature Limited. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.

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10.1038/s41589-019-0438-8

X325 SI after last review
© 2020 Springer Nature Limited. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.
Accepted author manuscript, 2.01 MB

Mechanistic insights into lytic polysaccharide monooxygenases
Walton, P. H. (Principal investigator) & Davies, G. J. (Co-investigator)
BBSRC (BIOTECHNOLOGY AND BIOLOGICAL SCIENCES RESEARCH COUNCIL)
1/04/18 → 31/03/23
Project: Research project (funded) › Research

Characterisation of LPMO AA16 family
Ciano, L. (Creator) & Walton, P. H. (Supervisor), University of York, 2018
DOI: 10.15124/a034974e-2782-415e-8b02-2b6e4098760e
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Cite this

Walton, P. H., Labourel, A., Frandsen, K. E. H., Zhang, F., Brouilly, N., Grisel, S., Haon, M., Ciano, L., Ropartz, D., Fanuel, M., Martin, F., Navarro, D., Rosso, M.-N., Tandrup, T., Bissaro, B., Johansen, K., Zerva, A., Henrissat, B., Lo Leggio, L., & Berrin, J.-G. (2020). A fungal family of lytic polysaccharide monooxygenase-like copper proteins. NATURE CHEMICAL BIOLOGY, 1-11. Article https://doi.org/10.1038/s41589-019-0438-8. https://doi.org/10.1038/s41589-019-0438-8

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abstract = "Lytic polysaccharide monooxygenases (LPMOs) are copper-containing enzymes that play a key role in the oxidative degradation of various biopolymers such as cellulose and chitin. While hunting for new LPMOs, we identified a new family of proteins, defined here as X325, in various fungal lineages. The three-dimensional structure of X325 revealed an overall LPMO fold and a His brace with an additional Asp ligand to Cu(II). Although LPMO-type activity of X325 members was initially expected, we demonstrated that X325 members do not perform oxidative cleavage of polysaccharides, establishing that X325s are not LPMOs. Investigations of the biological role of X325 in the ectomycorrhizal fungus Laccaria bicolor revealed exposure of the X325 protein at the interface between fungal hyphae and tree rootlet cells. Our results provide insights into a family of copper-containing proteins, which is widespread in the fungal kingdom and is evolutionarily related to LPMOs, but has diverged to biological functions other than polysaccharide degradation.",

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Walton, PH, Labourel, A, Frandsen, KEH, Zhang, F, Brouilly, N, Grisel, S, Haon, M, Ciano, L, Ropartz, D, Fanuel, M, Martin, F, Navarro, D, Rosso, M-N, Tandrup, T, Bissaro, B, Johansen, K, Zerva, A, Henrissat, B, Lo Leggio, L & Berrin, J-G 2020, 'A fungal family of lytic polysaccharide monooxygenase-like copper proteins', NATURE CHEMICAL BIOLOGY, pp. 1-11. https://doi.org/10.1038/s41589-019-0438-8

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AU - Walton, Paul Howard

AU - Labourel, Aurore

AU - Frandsen, Kristian E H

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AU - Brouilly, Nicolas

AU - Grisel, Sacha

AU - Haon, Mireille

AU - Ciano, Luisa

AU - Ropartz, David

AU - Fanuel, Mathieu

AU - Martin, Francis

AU - Navarro, David

AU - Rosso, Marie-Noëlle

AU - Tandrup, Tobias

AU - Bissaro, Bastien

AU - Johansen, Katja

AU - Zerva, Anastasia

AU - Henrissat, Bernard

AU - Lo Leggio, Leila

AU - Berrin, Jean-Guy

N1 - © 2020 Springer Nature Limited. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.

PY - 2020/1/13

Y1 - 2020/1/13

N2 - Lytic polysaccharide monooxygenases (LPMOs) are copper-containing enzymes that play a key role in the oxidative degradation of various biopolymers such as cellulose and chitin. While hunting for new LPMOs, we identified a new family of proteins, defined here as X325, in various fungal lineages. The three-dimensional structure of X325 revealed an overall LPMO fold and a His brace with an additional Asp ligand to Cu(II). Although LPMO-type activity of X325 members was initially expected, we demonstrated that X325 members do not perform oxidative cleavage of polysaccharides, establishing that X325s are not LPMOs. Investigations of the biological role of X325 in the ectomycorrhizal fungus Laccaria bicolor revealed exposure of the X325 protein at the interface between fungal hyphae and tree rootlet cells. Our results provide insights into a family of copper-containing proteins, which is widespread in the fungal kingdom and is evolutionarily related to LPMOs, but has diverged to biological functions other than polysaccharide degradation.

AB - Lytic polysaccharide monooxygenases (LPMOs) are copper-containing enzymes that play a key role in the oxidative degradation of various biopolymers such as cellulose and chitin. While hunting for new LPMOs, we identified a new family of proteins, defined here as X325, in various fungal lineages. The three-dimensional structure of X325 revealed an overall LPMO fold and a His brace with an additional Asp ligand to Cu(II). Although LPMO-type activity of X325 members was initially expected, we demonstrated that X325 members do not perform oxidative cleavage of polysaccharides, establishing that X325s are not LPMOs. Investigations of the biological role of X325 in the ectomycorrhizal fungus Laccaria bicolor revealed exposure of the X325 protein at the interface between fungal hyphae and tree rootlet cells. Our results provide insights into a family of copper-containing proteins, which is widespread in the fungal kingdom and is evolutionarily related to LPMOs, but has diverged to biological functions other than polysaccharide degradation.

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JO - NATURE CHEMICAL BIOLOGY

JF - NATURE CHEMICAL BIOLOGY

M1 - https://doi.org/10.1038/s41589-019-0438-8

ER -

A fungal family of lytic polysaccharide monooxygenase-like copper proteins

Abstract

Bibliographical note

Access to Document

Projects

Mechanistic insights into lytic polysaccharide monooxygenases

Datasets

Characterisation of LPMO AA16 family

Cite this