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Research Article

Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation

Jane W. Agger, Trine Isaksen, Anikó Várnai, Silvia Vidal-Melgosa, William G. T. Willats, Roland Ludwig, Svein J. Horn, Vincent G. H. Eijsink, and Bjørge Westereng
PNAS April 29, 2014 111 (17) 6287-6292; first published April 14, 2014; https://doi.org/10.1073/pnas.1323629111
Jane W. Agger
aDepartment of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences (NMBU), 1432 Aas, Norway;
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Trine Isaksen
aDepartment of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences (NMBU), 1432 Aas, Norway;
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Anikó Várnai
aDepartment of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences (NMBU), 1432 Aas, Norway;
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Silvia Vidal-Melgosa
bDepartment of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen,1871 Frederiksberg, Denmark;
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William G. T. Willats
bDepartment of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen,1871 Frederiksberg, Denmark;
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Roland Ludwig
cDepartment of Food Sciences and Technology, BOKU–University of Natural Resources and Life Sciences, 1190 Vienna, Austria; and
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Svein J. Horn
aDepartment of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences (NMBU), 1432 Aas, Norway;
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Vincent G. H. Eijsink
aDepartment of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences (NMBU), 1432 Aas, Norway;
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  • For correspondence: vincent.eijsink@nmbu.no
Bjørge Westereng
aDepartment of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences (NMBU), 1432 Aas, Norway;
bDepartment of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen,1871 Frederiksberg, Denmark;
dDepartment of Geosciences and Natural Resource Management, Faculty of Science, University of Copenhagen, 1958 Frederiksberg C, Denmark
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  1. Edited by Arnold L. Demain, Drew University, Madison, NJ, and approved March 21, 2014 (received for review December 20, 2013)

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Significance

Plant cell walls are recalcitrant copolymeric structures mainly comprising polysaccharides and lignin. Enzymatic degradation of the polysaccharides is a crucial step in biorefining of biomass. Recently, it was discovered that nature employs copper-dependent redox enzymes called lytic polysaccharide monoxoygenases (LPMOs) to promote degradation of the most recalcitrant and crystalline of these polysaccharides, cellulose. By carrying out oxidative cleavage of otherwise inaccessible cellulose chains, LPMOs create access points for classical hydrolytic enzymes such as cellulases. Intriguingly, the genomes of biomass degrading microorganisms encode a plethora of LPMOs (up to over 40). To our knowledge, we demonstrate for the first time that LPMOs act on hemicelluloses. This finding dramatically widens the scope of LPMOs and oxidative processes in plant cell wall degradation and biorefining.

Abstract

The recently discovered lytic polysaccharide monooxygenases (LPMOs) are known to carry out oxidative cleavage of glycoside bonds in chitin and cellulose, thus boosting the activity of well-known hydrolytic depolymerizing enzymes. Because biomass-degrading microorganisms tend to produce a plethora of LPMOs, and considering the complexity and copolymeric nature of the plant cell wall, it has been speculated that some LPMOs may act on other substrates, in particular the hemicelluloses that tether to cellulose microfibrils. We demonstrate that an LPMO from Neurospora crassa, NcLPMO9C, indeed degrades various hemicelluloses, in particular xyloglucan. This activity was discovered using a glycan microarray-based screening method for detection of substrate specificities of carbohydrate-active enzymes, and further explored using defined oligomeric hemicelluloses, isolated polymeric hemicelluloses and cell walls. Products generated by NcLPMO9C were analyzed using high performance anion exchange chromatography and multidimensional mass spectrometry. We show that NcLPMO9C generates oxidized products from a variety of substrates and that its product profile differs from those of hydrolytic enzymes acting on the same substrates. The enzyme particularly acts on the glucose backbone of xyloglucan, accepting various substitutions (xylose, galactose) in almost all positions. Because the attachment of xyloglucan to cellulose hampers depolymerization of the latter, it is possible that the beneficial effect of the LPMOs that are present in current commercial cellulase mixtures in part is due to hitherto undetected LPMO activities on recalcitrant hemicellulose structures.

  • biorefinery
  • metallo enzymes
  • GH61
  • CBM33

Footnotes

  • ↵1T.I. and A.V. contributed equally to this manuscript.

  • ↵2To whom correspondence should be addressed. E-mail: vincent.eijsink{at}nmbu.no.
  • Author contributions: J.W.A., S.V.-M., W.G.T.W., V.G.H.E., and B.W. designed research; J.W.A., T.I., A.V., S.V.-M., and B.W. performed research; J.W.A., S.V.-M., W.G.T.W., R.L., and B.W. contributed new reagents/analytic tools; J.W.A., A.V., W.G.T.W., S.J.H., V.G.H.E., and B.W. analyzed data; and J.W.A., T.I., A.V., S.V.-M., W.G.T.W., R.L., S.J.H., V.G.H.E., and B.W. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1323629111/-/DCSupplemental.

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Discovery of LPMO activity on hemicelluloses
Jane W. Agger, Trine Isaksen, Anikó Várnai, Silvia Vidal-Melgosa, William G. T. Willats, Roland Ludwig, Svein J. Horn, Vincent G. H. Eijsink, Bjørge Westereng
Proceedings of the National Academy of Sciences Apr 2014, 111 (17) 6287-6292; DOI: 10.1073/pnas.1323629111

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Discovery of LPMO activity on hemicelluloses
Jane W. Agger, Trine Isaksen, Anikó Várnai, Silvia Vidal-Melgosa, William G. T. Willats, Roland Ludwig, Svein J. Horn, Vincent G. H. Eijsink, Bjørge Westereng
Proceedings of the National Academy of Sciences Apr 2014, 111 (17) 6287-6292; DOI: 10.1073/pnas.1323629111
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