Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases

Kristian E H Frandsen; Morten Tovborg; Christian I. Jørgensen; Nikolai Spodsberg; Marie-Noëlle Rosso; Glyn R Hemsworth; Elspeth F Garman; Geoffrey W Grime; Jens-Christian N Poulsen; Tanveer S. Batth; Shingo Miyauchi; Anna Lipzen; Chris Daum; Igor V Grigoriev; Katja S Johansen; Bernard Henrissat; Jean-Guy Berrin; Leila Lo Leggio

doi:10.1074/jbc.ra119.009223

Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases

Kristian E H Frandsen, Morten Tovborg, Christian I. Jørgensen, Nikolai Spodsberg, Marie-Noëlle Rosso, Glyn R Hemsworth, Elspeth F Garman, Geoffrey W Grime, Jens-Christian N Poulsen, Tanveer S. Batth, Shingo Miyauchi, Anna Lipzen, Chris Daum, Igor V Grigoriev, Katja S Johansen, Bernard Henrissat, Jean-Guy Berrin, Leila Lo Leggio

9 Citationer (Scopus)

Abstract

Lytic polysaccharide monooxygenases (LPMOs) are redoxenzymes involved in biomass degradation. All characterized LPMOs possess an active site of two highly conserved histidine residues coordinating a copper ion (the histidine brace), which are essential for LPMO activity. However, some protein sequences that belong to the AA9 LPMO family display a natural N-terminal His to Arg substitution (Arg-AA9). These are found almost entirely in the phylogenetic fungal class Agaricomycetes, associated with wood decay, but no function has been demonstrated for any Arg-AA9. Through bioinformatics, transcriptomic, and proteomic analyses we present data, which suggest that Arg-AA9 proteins could have a hitherto unidentified role in fungal degradation of lignocellulosic biomass in conjunction with other secreted fungal enzymes. We present the first structure of an ArgAA9, LsAA9B, a naturally occurring protein from Lentinus similis. The LsAA9B structure reveals gross changes in the region equivalent to the canonical LPMO copper-binding site, whereas features implicated in carbohydrate binding in AA9 LPMOs have been maintained. We obtained a structure of LsAA9B with xylotetraose bound on the surface of the protein although with a considerably different binding mode compared with other AA9 complex structures. In addition, we have found indications of protein phosphorylationneartheN-terminalArg andthe carbohydrate-binding site, for which the potential function is currently unknown. Our results are strong evidence that Arg-AA9s function markedly different from canonical AA9 LPMO, but nonetheless, may play a role in fungal conversion of lignocellulosic biomass.

Originalsprog	Engelsk
Tidsskrift	The Journal of Biological Chemistry
Vol/bind	294
Sider (fra-til)	17117-17130
Antal sider	24
ISSN	0021-9258
DOI	https://doi.org/10.1074/jbc.ra119.009223
Status	Udgivet - 8 nov. 2019

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10.1074/jbc.ra119.009223

http://www.jbc.org/content/294/45/17117.full.pdfLicens: CC BY

Citationsformater

Frandsen, K. E. H., Tovborg, M., Jørgensen, C. I., Spodsberg, N., Rosso, M.-N., Hemsworth, G. R., Garman, E. F., Grime, G. W., Poulsen, J.-C. N., Batth, T. S., Miyauchi, S., Lipzen, A., Daum, C., Grigoriev, I. V., Johansen, K. S., Henrissat, B., Berrin, J.-G., & Lo Leggio, L. (2019). Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases. The Journal of Biological Chemistry, 294, 17117-17130. https://doi.org/10.1074/jbc.ra119.009223

Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases. / Frandsen, Kristian E H; Tovborg, Morten; Jørgensen, Christian I. et al.
I: The Journal of Biological Chemistry, Bind 294, 08.11.2019, s. 17117-17130.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

Frandsen, KEH, Tovborg, M, Jørgensen, CI, Spodsberg, N, Rosso, M-N, Hemsworth, GR, Garman, EF, Grime, GW, Poulsen, J-CN, Batth, TS, Miyauchi, S, Lipzen, A, Daum, C, Grigoriev, IV, Johansen, KS, Henrissat, B, Berrin, J-G & Lo Leggio, L 2019, 'Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases', The Journal of Biological Chemistry, bind 294, s. 17117-17130. https://doi.org/10.1074/jbc.ra119.009223

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title = "Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases",

abstract = "Lytic polysaccharide monooxygenases (LPMOs) are redoxenzymes involved in biomass degradation. All characterized LPMOs possess an active site of two highly conserved histidine residues coordinating a copper ion (the histidine brace), which are essential for LPMO activity. However, some protein sequences that belong to the AA9 LPMO family display a natural N-terminal His to Arg substitution (Arg-AA9). These are found almost entirely in the phylogenetic fungal class Agaricomycetes, associated with wood decay, but no function has been demonstrated for any Arg-AA9. Through bioinformatics, transcriptomic, and proteomic analyses we present data, which suggest that Arg-AA9 proteins could have a hitherto unidentified role in fungal degradation of lignocellulosic biomass in conjunction with other secreted fungal enzymes. We present the first structure of an ArgAA9, LsAA9B, a naturally occurring protein from Lentinus similis. The LsAA9B structure reveals gross changes in the region equivalent to the canonical LPMO copper-binding site, whereas features implicated in carbohydrate binding in AA9 LPMOs have been maintained. We obtained a structure of LsAA9B with xylotetraose bound on the surface of the protein although with a considerably different binding mode compared with other AA9 complex structures. In addition, we have found indications of protein phosphorylationneartheN-terminalArg andthe carbohydrate-binding site, for which the potential function is currently unknown. Our results are strong evidence that Arg-AA9s function markedly different from canonical AA9 LPMO, but nonetheless, may play a role in fungal conversion of lignocellulosic biomass.",

author = "Frandsen, {Kristian E H} and Morten Tovborg and J{\o}rgensen, {Christian I.} and Nikolai Spodsberg and Marie-No{\"e}lle Rosso and Hemsworth, {Glyn R} and Garman, {Elspeth F} and Grime, {Geoffrey W} and Poulsen, {Jens-Christian N} and Batth, {Tanveer S.} and Shingo Miyauchi and Anna Lipzen and Chris Daum and Grigoriev, {Igor V} and Johansen, {Katja S} and Bernard Henrissat and Jean-Guy Berrin and {Lo Leggio}, Leila",

note = "Published under license by The American Society for Biochemistry and Molecular Biology, Inc.",

year = "2019",

month = nov,

day = "8",

doi = "10.1074/jbc.ra119.009223",

language = "English",

volume = "294",

pages = "17117--17130",

journal = "The Journal of Biological Chemistry",

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publisher = "American Society for Biochemistry and Molecular Biology, Inc.",

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TY - JOUR

T1 - Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases

AU - Frandsen, Kristian E H

AU - Tovborg, Morten

AU - Jørgensen, Christian I.

AU - Spodsberg, Nikolai

AU - Rosso, Marie-Noëlle

AU - Hemsworth, Glyn R

AU - Garman, Elspeth F

AU - Grime, Geoffrey W

AU - Poulsen, Jens-Christian N

AU - Batth, Tanveer S.

AU - Miyauchi, Shingo

AU - Lipzen, Anna

AU - Daum, Chris

AU - Grigoriev, Igor V

AU - Johansen, Katja S

AU - Henrissat, Bernard

AU - Berrin, Jean-Guy

AU - Lo Leggio, Leila

N1 - Published under license by The American Society for Biochemistry and Molecular Biology, Inc.

PY - 2019/11/8

Y1 - 2019/11/8

N2 - Lytic polysaccharide monooxygenases (LPMOs) are redoxenzymes involved in biomass degradation. All characterized LPMOs possess an active site of two highly conserved histidine residues coordinating a copper ion (the histidine brace), which are essential for LPMO activity. However, some protein sequences that belong to the AA9 LPMO family display a natural N-terminal His to Arg substitution (Arg-AA9). These are found almost entirely in the phylogenetic fungal class Agaricomycetes, associated with wood decay, but no function has been demonstrated for any Arg-AA9. Through bioinformatics, transcriptomic, and proteomic analyses we present data, which suggest that Arg-AA9 proteins could have a hitherto unidentified role in fungal degradation of lignocellulosic biomass in conjunction with other secreted fungal enzymes. We present the first structure of an ArgAA9, LsAA9B, a naturally occurring protein from Lentinus similis. The LsAA9B structure reveals gross changes in the region equivalent to the canonical LPMO copper-binding site, whereas features implicated in carbohydrate binding in AA9 LPMOs have been maintained. We obtained a structure of LsAA9B with xylotetraose bound on the surface of the protein although with a considerably different binding mode compared with other AA9 complex structures. In addition, we have found indications of protein phosphorylationneartheN-terminalArg andthe carbohydrate-binding site, for which the potential function is currently unknown. Our results are strong evidence that Arg-AA9s function markedly different from canonical AA9 LPMO, but nonetheless, may play a role in fungal conversion of lignocellulosic biomass.

AB - Lytic polysaccharide monooxygenases (LPMOs) are redoxenzymes involved in biomass degradation. All characterized LPMOs possess an active site of two highly conserved histidine residues coordinating a copper ion (the histidine brace), which are essential for LPMO activity. However, some protein sequences that belong to the AA9 LPMO family display a natural N-terminal His to Arg substitution (Arg-AA9). These are found almost entirely in the phylogenetic fungal class Agaricomycetes, associated with wood decay, but no function has been demonstrated for any Arg-AA9. Through bioinformatics, transcriptomic, and proteomic analyses we present data, which suggest that Arg-AA9 proteins could have a hitherto unidentified role in fungal degradation of lignocellulosic biomass in conjunction with other secreted fungal enzymes. We present the first structure of an ArgAA9, LsAA9B, a naturally occurring protein from Lentinus similis. The LsAA9B structure reveals gross changes in the region equivalent to the canonical LPMO copper-binding site, whereas features implicated in carbohydrate binding in AA9 LPMOs have been maintained. We obtained a structure of LsAA9B with xylotetraose bound on the surface of the protein although with a considerably different binding mode compared with other AA9 complex structures. In addition, we have found indications of protein phosphorylationneartheN-terminalArg andthe carbohydrate-binding site, for which the potential function is currently unknown. Our results are strong evidence that Arg-AA9s function markedly different from canonical AA9 LPMO, but nonetheless, may play a role in fungal conversion of lignocellulosic biomass.

U2 - 10.1074/jbc.ra119.009223

DO - 10.1074/jbc.ra119.009223

M3 - Journal article

C2 - 31471321

SN - 0021-9258

VL - 294

SP - 17117

EP - 17130

JO - The Journal of Biological Chemistry

JF - The Journal of Biological Chemistry

ER -

Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases

Abstract

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