Carbohydrate-aromatic interface and molecular architecture of lignocellulose

Abstract

Plant cell walls constitute the majority of lignocellulosic biomass and serve as a renewable resource of biomaterials and biofuel. Extensive interactions between polysaccharides and the aromatic polymer lignin make lignocellulose recalcitrant to enzymatic hydrolysis, but this polymer network remains poorly understood. Here we interrogate the nanoscale assembly of lignocellulosic components in plant stems using solid-state nuclear magnetic resonance and dynamic nuclear polarization approaches. We show that the extent of glycan-aromatic association increases sequentially across grasses, hardwoods, and softwoods. Lignin principally packs with the xylan in a non-flat conformation via non-covalent interactions and partially binds the junction of flat-ribbon xylan and cellulose surface as a secondary site. All molecules are homogeneously mixed in softwoods; this unique feature enables water retention even around the hydrophobic aromatics. These findings unveil the principles of polymer interactions underlying the heterogeneous architecture of lignocellulose, which may guide the rational design of more digestible plants and more efficient biomass-conversion pathways.

Structure of In Vitro-Synthesized Cellulose Fibrils Viewed by Cryo-Electron Tomography and 13C Natural-Abundance Dynamic Nuclear Polarization Solid-State NMR

“…The 87.6 ppm signal has a similar chemical shift to the type-c cellulose recently identified in intact plant cell walls. 34 − 36 In plants, this special conformer belongs to some glucan chains that are deeply embedded in the core of a fibril, thus becoming spatially separated from surface chains. These chains cannot be accommodated by a small 18-chain microfibril; therefore, they might be created during the microfibril bundling process, which produces larger fibrils.…”

“…Second, including the contribution of the weak peak at 87.6 ppm increased the content of interior cellulose to 35%. This minor component probably correlates with the type-c cellulose in plant cell walls, which belongs to a special form of glucan chains deeply embedded in the center of a bundle of microfibrils. , The increase in the surface-to-interior ratio might reflect the structural effect of the bundling of microfibrils. Third, including the area of the 81.5 ppm peak (likely from some highly disordered surface chains) in the calculation will bring down the percentage of interior cellulose back to 29%.…”

“…Recently, multidimensional solid-state NMR techniques have shown their capability of revealing the molecular structure of cellulose and its interactions with other biopolymers (such as hemicellulose, pectin, and lignin) in native plant cell walls and carbohydrate-based materials. − By coupling 13 C labeling of samples and high-field NMR, seven types of glucose units were consistently identified in the CMFs across the cell walls of a variety of plant genera, including Arabidopsis, Brachypodium, maize, rice, switchgrass, poplar, eucalyptus, and spruce. − None of these glucose units follow the 13 C chemical shifts of the bulk allomorphs, Iα and Iβ structures, revealing a substantially deviated structure of cellulose when placed in the native context. However, the expected signals of Iα and Iβ allomorphs have been recently observed in cotton, indicating that model crystal structures are only possible in highly crystalline cellulose with large crystallites .…”

Lignin p-Hydroxybenzoylation Is Negatively Correlated With Syringyl Units in Poplar

“…The observation that p-hydroxybenzoylation correlates with xylan but not lignin nor cellulose contents could be an indication that lignin-bound pHB groups have an analogous role to xylan modifications. Indeed, it has been shown that lignin interacts primarily with xylan in poplar cell walls (Kirui et al, 2022), and it is known that lignin acylation impacts hydrophobicity and solubility by increasing the number of free phenolic groups (Lapierre et al, 2021). In addition, p-hydroxybenzoylation alters the structure of lignin by favouring β-aryl ether interunit linkages (Lu et al, 2015;Mottiar, 2021).…”

Atomistic Origins of Biomass Recalcitrance in Organosolv Pretreatment

“…The largest component within the plant cell wall is the secondary cell wall, made primarily from the polysaccharides cellulose (∼ 50%) and hemicellulose (∼ 20%), along with polyphenolic polymer lignin (∼ 30%) [4]. Emerging NMR evidence suggests that all three biopolymers form close interactions within the plant cell wall [5,6,7]. With an estimated global yield of 1.3 billion tons per year [8], these biomass components are an abundant and renewable bioeconomy feedstock for plant-based materials [4,9].…”