The formation of covalent linkages via the oxocarbenium intermediate in lignocellulosic biomass

Elucidating molecular origins of plant recalcitrance is critical for developing novel and atom-efficient strategies for lignocellulosic biomass (LCB) valorization. In particular, understanding the formation of covalent, lignin-carbohydrate complex (LCC) linkages is crucial because these interactions are known to significantly contribute to plant recalcitrance. In this work, a new mechanism for the formation of LCC linkages in LCB is explored. Our proposal is based on the formation of the oxocarbenium intermediate in sugar moieties in hemicellulose and the subsequent formation of glycosidic bonds between polysaccharides and lignin. We applied density functional theory calculations to monosaccharides and monolignol molecules serving as model precursors for LCB. Namely, mannopyranose, xylopyranose, arabinofuranose, and glucopyranuronic acid were used as hemicellulose models; p-coumaryl alcohol, coniferyl alcohol, and sinapyl alcohol were employed as lignin models. Computations without the presence of explicit water molecules predict the stable formation of the proposed glycosidic bonds between all lignin and all sugar models, with some exceptions for mannopyranose and arabinofuranose. Whereas including explicit water molecules showed that, for all systems, the formation of LCC bonds is more thermodynamically favourable than in the absence of water or when using implicit solvent models. In addition, the explicit solvent models indicate that hydrogen bonding between water and organic molecules promotes the formation of more stable LCC bonds. Finally, transition states and intermediates associated with the formation of oxocarbenium ions were computationally found for mannopyranose and xylopyranose, allowing us to evaluate the kinetics of LCC linkage formation for major components of hemicellulose in the secondary cell walls of plants. These results, in combination with recent experimental evidence on hemicellulose-lignin interactions in native biomass, suggest that glycosylation reactions via the oxocarbenium intermediate can occur in the secondary cell walls of plants. Specifically, the hydrated nature of the hemicellulose matrix and the proximity of lignin to hemicellulose in native LCB provides the necessary conditions for the formation of the LCC linkages proposed herein. Overall, this study provides further evidence for the formation of covalent LCC linkages in LCB.