Nanomechanics of cellulose deformation reveal molecular defects that facilitate natural deconstruction

Abstract

Technologies surrounding utilization of cellulosic materials have been integral to human society for millennia. In many materials, controlled introduction of defects provides a means to tailor properties, introduce reactivity, and modulate functionality for various applications. The importance of defects in defining the behavior of cellulose is becoming increasingly recognized. However, fully exploiting defects in cellulose to benefit biobased materials and conversion applications will require an improved understanding of the mechanisms of defect induction and corresponding molecular-level consequences. We have identified a fundamental relationship between the macromolecular structure and mechanical behavior of cellulose nanofibrils whereby molecular defects may be induced when the fibrils are subjected to bending stress exceeding a certain threshold. By nanomanipulation, imaging, and molecular modeling, we demonstrate that cellulose nanofibrils tend to form kink defects in response to bending stress, and that these macromolecular features are often accompanied by breakages in the glucan chains. Direct observation of deformed cellulose fibrils following partial enzymatic digestion reveals that processive cellulases exploit these defects as initiation sites for hydrolysis. Collectively, our findings provide a refined understanding of the interplay between the structure, mechanics, and reactivity of cellulose assemblies.

Interfacial molecular interactions of cellobiohydrolase Cel7A and its variants on cellulose

“…Moreover, computational modeling based on transmission electron microscopy revealed that cellulose microfibrils kink along their lengths in their energy minimized state [40]. Ciesielski et al proposed that highly crystalline cellulose fibrils kink to release internal stresses [41]; we speculate that we observed this stress release due to the cellulose fibrils being actively hydrolyzed. Although the process of kinking was only observed twice, kinked fibrils were frequently observed in the experimental samples.…”

The plant cell wall: Biosynthesis, construction, and functions

“…The xyloglucan backbone is synthesized by cellulose synthase‐like C (CslC) family members; the Arabidopsis cslc4 mutant and the quintuple mutant cslc4 cslc5 cslc6 cslc8 cslc12 have undetectable xyloglucan levels (Cocuron et al, 2007; Kim et al, 2020). The enzymatic activity of AtCslC4 has been examined (Cocuron et al, 2007).…”

A novel supra coarse-grained model for cellulose

“…Cellulose has been the subject of many molecular simulation studies. Some of these studies focus only at the surface phenomena and modifications of CNC, (Chen et al 2017;Zhou et al 2015;Bergenstråhle et al 2008;Paajanen et al 2016;Chundawat et al 2011) while many others simulate whole CNC, both at atomistic (Chen et al 2017;Zhou et al 2015;Bergenstråhle et al 2008;Paajanen et al 2016;Chundawat et al 2011;Matthews et al 2006;Conley et al 2016;Oehme et al 2015;Djahedi et al 2015;Paajanen et al 2019;Ciesielski et al 2019) and coarsegrained representations (López et al 2009;Wohlert and Berglund 2011;López et al 2015;Mehandzhiyski and Zozoulenko 2019;Glass et al 2012;Fan and Maranas 2015;Markutsya et al 2013;Shishehbor et al 2018;Shishehbor and Zavattieri 2019;Ramezani and Golchinfar 2019;Srinivas et al 2011;Poma et al 2015Poma et al , 2016Poma et al , 2017. All-atom molecular dynamics (AA-MD) studies are able to simulate the crystal structure of cellulose in a perfect agreement with the experimental crystal structure of different cellulose allomorphs and provide a detailed atomistic picture for the structure and dynamics of CNC (Chundawat et al 2011).…”