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Title: 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.

Authors:
; ; ; ; ; ORCiD logo; ORCiD logo; ;
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1509915
Alternate Identifier(s):
OSTI ID: 1512662
Report Number(s):
NREL/JA-2700-73748
Journal ID: ISSN 0027-8424; /pnas/116/20/9825.atom
Grant/Contract Number:  
AC36-08GO28308
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 20; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; cellulose; cellulases; atomic force microscopy; molecular dynamics; quantum mechanics

Citation Formats

Ciesielski, Peter N., Wagner, Ryan, Bharadwaj, Vivek S., Killgore, Jason, Mittal, Ashutosh, Beckham, Gregg T., Decker, Stephen R., Himmel, Michael E., and Crowley, Michael F. Nanomechanics of cellulose deformation reveal molecular defects that facilitate natural deconstruction. United States: N. p., 2019. Web. doi:10.1073/pnas.1900161116.
Ciesielski, Peter N., Wagner, Ryan, Bharadwaj, Vivek S., Killgore, Jason, Mittal, Ashutosh, Beckham, Gregg T., Decker, Stephen R., Himmel, Michael E., & Crowley, Michael F. Nanomechanics of cellulose deformation reveal molecular defects that facilitate natural deconstruction. United States. doi:10.1073/pnas.1900161116.
Ciesielski, Peter N., Wagner, Ryan, Bharadwaj, Vivek S., Killgore, Jason, Mittal, Ashutosh, Beckham, Gregg T., Decker, Stephen R., Himmel, Michael E., and Crowley, Michael F. Mon . "Nanomechanics of cellulose deformation reveal molecular defects that facilitate natural deconstruction". United States. doi:10.1073/pnas.1900161116.
@article{osti_1509915,
title = {Nanomechanics of cellulose deformation reveal molecular defects that facilitate natural deconstruction},
author = {Ciesielski, Peter N. and Wagner, Ryan and Bharadwaj, Vivek S. and Killgore, Jason and Mittal, Ashutosh and Beckham, Gregg T. and Decker, Stephen R. and Himmel, Michael E. and Crowley, Michael F.},
abstractNote = {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.},
doi = {10.1073/pnas.1900161116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 20,
volume = 116,
place = {United States},
year = {2019},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1900161116

Citation Metrics:
Cited by: 5 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: Probing mechanical deformation at the nanoscale reveals reversible and irreversible nature of cellulose kinks. (A–D′) AFM images of cellulose nanofibrils before and after a series of lithographic lateral manipulations with the AFM tip demonstrate three typical responses. The arrow in each image indicates the location and direction ofmore » applied force. (A–A′′) Multiple kinks were induced along the length of the fibril. (B–B′′) Complete breakage of the fibril was achieved by applying manipulation to the vicinity of an existing kink defect, while the fibril was strongly adhered to the substrate. (C–C′′) A previously kinked fibril was straightened, indicating that the kinks observed in C and C′ still maintain some degree of molecular connectivity. (D) A cellulose nanofibril suspended over a 200-nm pore in track-etched polycarbonate (TEPC). (D′) Kink defect formed in the same nanofibril shown in D after AFM indentation at 48-nN applied load. (Inset) Comparison of the topographic line profile of the nanofibril before and after indentation, clearly revealing the presence of a mechanically induced kink at the supporting pore wall. (E) Approach and retract indentation curves for the particular indentation step that induced kinking in the nanofibril. After reaching the maximum force Fmax in the approach curve the cellulose forms a kink, allowing the probe tip to slip into the pore wall. (F) AFM indentation and bending measurements along the length of a nanofibril were fit to a beam model to calculate deformation stress.« less

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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.