Structural and electronic determinants of lytic polysaccharide monooxygenase reactivity on polysaccharide substrates

TY - JOUR

T1 - Structural and electronic determinants of lytic polysaccharide monooxygenase reactivity on polysaccharide substrates

AU - Simmons, Thomas J

AU - Frandsen, Kristian E H

AU - Ciano, Luisa

AU - Tryfona, Theodora

AU - Lenfant, Nicolas

AU - Poulsen, Jens-Christian N.

AU - Wilson, Louis F. L.

AU - Tandrup, Tobias

AU - Tovborg, Morten

AU - Schnorr, Kirk

AU - Johansen, Katja Salomon

AU - Henrissat, Bernard

AU - Walton, Paul Howard

AU - Lo Leggio, Leila

AU - Dupree, Paul

N1 - © The Author(s) 2017.

PY - 2017/10/20

Y1 - 2017/10/20

N2 - Lytic polysaccharide monooxygenases (LPMOs) are industrially important copper-dependent enzymes that oxidatively cleave polysaccharides. Here we present a functional and structural characterization of two closely related AA9-family LPMOs from Lentinus similis (LsAA9A) and Collariella virescens (CvAA9A). LsAA9A and CvAA9A cleave a range of polysaccharides, including cellulose, xyloglucan, mixed-linkage glucan and glucomannan. LsAA9A additionally cleaves isolated xylan substrates. The structures of CvAA9A and of LsAA9A bound to cellulosic and non-cellulosic oligosaccharides provide insight into the molecular determinants of their specificity. Spectroscopic measurements reveal differences in copper co-ordination upon the binding of xylan and glucans. LsAA9A activity is less sensitive to the reducing agent potential when cleaving xylan, suggesting that distinct catalytic mechanisms exist for xylan and glucan cleavage. Overall, these data show that AA9 LPMOs can display different apparent substrate specificities dependent upon both productive protein–carbohydrate interactions across a binding surface and also electronic considerations at the copper active site.

AB - Lytic polysaccharide monooxygenases (LPMOs) are industrially important copper-dependent enzymes that oxidatively cleave polysaccharides. Here we present a functional and structural characterization of two closely related AA9-family LPMOs from Lentinus similis (LsAA9A) and Collariella virescens (CvAA9A). LsAA9A and CvAA9A cleave a range of polysaccharides, including cellulose, xyloglucan, mixed-linkage glucan and glucomannan. LsAA9A additionally cleaves isolated xylan substrates. The structures of CvAA9A and of LsAA9A bound to cellulosic and non-cellulosic oligosaccharides provide insight into the molecular determinants of their specificity. Spectroscopic measurements reveal differences in copper co-ordination upon the binding of xylan and glucans. LsAA9A activity is less sensitive to the reducing agent potential when cleaving xylan, suggesting that distinct catalytic mechanisms exist for xylan and glucan cleavage. Overall, these data show that AA9 LPMOs can display different apparent substrate specificities dependent upon both productive protein–carbohydrate interactions across a binding surface and also electronic considerations at the copper active site.

KW - Catalytic Domain

KW - Copper/chemistry

KW - Electron Spin Resonance Spectroscopy

KW - Fungal Proteins/chemistry

KW - Mixed Function Oxygenases/chemistry

KW - Models, Molecular

KW - Polyporaceae/enzymology

KW - Polysaccharides/chemistry

KW - Sordariales/enzymology

KW - Substrate Specificity

UR - http://www.scopus.com/inward/record.url?scp=85032223646&partnerID=8YFLogxK

U2 - 10.1038/s41467-017-01247-3

DO - 10.1038/s41467-017-01247-3

M3 - Article

SN - 2041-1723

VL - 8

JO - Nature Communications

JF - Nature Communications

M1 - 1064 (2017)

ER -