Xylan inhibition of cellulase binding and processivity observed at single-molecule resolution

Zexer, Nerya; Paradiso, Alec; Nong, Daguan; Haviland, Zachary K.; Hancock, William O.; Anderson, Charles T.

doi:10.1039/D4SU00006D

Title: Xylan inhibition of cellulase binding and processivity observed at single-molecule resolution

Journal Article · 04 April 2024 · RSC Sustainability

DOI: https://doi.org/10.1039/D4SU00006D · OSTI ID:2326124

Zexer, Nerya ^[1]; Paradiso, Alec ^[1]; Nong, Daguan ^[2]; Haviland, Zachary K. ^[2]; Hancock, William O. ^[2];

^[1]

Department of Biology, Pennsylvania State University, University Park, Pennsylvania, USA
Department of Biomedical Engineering, Pennsylvania State University, University Park, Pennsylvania, USA

Efficient cellulose degradation by cellulase enzymes is crucial for using lignocellulosic biomass in bioenergy production. Single-molecule microscopy showed that xylan hinders the efficiency of cellulase by inhibiting its binding to cellulose and impeding the processivity of bound enzyme molecules.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: NONE; SC0019065

OSTI ID:: 2326124

Journal Information:: RSC Sustainability, Journal Name: RSC Sustainability Journal Issue: 4 Vol. 2; ISSN 2753-8125; ISSN RSSUAN

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (31)

The effect of hemicellulose on the binding and activity of cellobiohydrolase I, Cel7A, from Trichoderma reesei to cellulose Malgas, S.; Kwanya Minghe, V. M.; Pletschke, B. I. Cellulose, Vol. 27, Issue 2 https://doi.org/10.1007/s10570-019-02848-5	journal	November 2019
Crystalline cellulose degradation: new insight into the function of cellobiohydrolases Teeri, Tuula T. Trends in Biotechnology, Vol. 15, Issue 5, p. 160-167 https://doi.org/10.1016/S0167-7799(97)01032-9	journal	May 1997
Xylans inhibit enzymatic hydrolysis of lignocellulosic materials by cellulases Zhang, Junhua; Tang, Ming; Viikari, Liisa Bioresource Technology, Vol. 121 https://doi.org/10.1016/j.biortech.2012.07.010	journal	October 2012
Tracking Single Particles and Elongated Filaments with Nanometer Precision Ruhnow, Felix; Zwicker, David; Diez, Stefan Biophysical Journal, Vol. 100, Issue 11 https://doi.org/10.1016/j.bpj.2011.04.023	journal	June 2011
Xylan adsorption on cellulose: Preferred alignment and local surface immobilizing effect Heinonen, Emilia; Henriksson, Gunnar; Lindström, Mikael E. Carbohydrate Polymers, Vol. 285 https://doi.org/10.1016/j.carbpol.2022.119221	journal	June 2022
Nanoscale dynamics of cellulose digestion by the cellobiohydrolase TrCel7A Haviland, Zachary K.; Nong, Daguan; Vasquez Kuntz, Kate L. Journal of Biological Chemistry, Vol. 297, Issue 3 https://doi.org/10.1016/j.jbc.2021.101029	journal	September 2021
An update on xylan structure, biosynthesis, and potential commercial applications Curry, Thomas M.; Peña, Maria J.; Urbanowicz, Breeanna R. The Cell Surface, Vol. 9 https://doi.org/10.1016/j.tcsw.2023.100101	journal	December 2023
Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR Simmons, Thomas J.; Mortimer, Jenny C.; Bernardinelli, Oigres D. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13902	journal	December 2016
Colocalization of fluorescent markers in confocal microscope images of plant cells French, Andrew P.; Mills, Steven; Swarup, Ranjan Nature Protocols, Vol. 3, Issue 4 https://doi.org/10.1038/nprot.2008.31	journal	March 2008
Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR Kang, Xue; Kirui, Alex; Dickwella Widanage, Malitha C. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-018-08252-0	journal	January 2019
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls Grantham, Nicholas J.; Wurman-Rodrich, Joel; Terrett, Oliver M. Nature Plants, Vol. 3, Issue 11 https://doi.org/10.1038/s41477-017-0030-8	journal	October 2017
Xylan-based nanocompartments orchestrate plant vessel wall patterning Wang, Hang; Yang, Hanlei; Wen, Zhao Nature Plants, Vol. 8, Issue 3 https://doi.org/10.1038/s41477-022-01113-1	journal	March 2022
Comparison of different pretreatments on the synergistic effect of cellulase and xylanase during the enzymatic hydrolysis of sugarcane bagasse Huang, Chao; Zhao, Cheng; Li, Hailong RSC Advances, Vol. 8, Issue 54 https://doi.org/10.1039/C8RA05047C	journal	January 2018
The dissociation mechanism of processive cellulases Vermaas, Josh V.; Kont, Riin; Beckham, Gregg T. Proceedings of the National Academy of Sciences, Vol. 116, Issue 46 https://doi.org/10.1073/pnas.1913398116	journal	October 2019
Binding Preferences, Surface Attachment, Diffusivity, and Orientation of a Family 1 Carbohydrate-binding Module on Cellulose Nimlos, Mark R.; Beckham, Gregg T.; Matthews, James F. Journal of Biological Chemistry, Vol. 287, Issue 24 https://doi.org/10.1074/jbc.M112.358184	journal	April 2012
Kinetics of Cellobiohydrolase (Cel7A) Variants with Lowered Substrate Affinity Kari, Jeppe; Olsen, Johan; Borch, Kim Journal of Biological Chemistry, Vol. 289, Issue 47 https://doi.org/10.1074/jbc.M114.604264	journal	September 2014
Recent developments in the production and applications of bacterial cellulose fibers and nanocrystals Reiniati, Isabela; Hrymak, Andrew N.; Margaritis, Argyrios Critical Reviews in Biotechnology, Vol. 37, Issue 4 https://doi.org/10.1080/07388551.2016.1189871	journal	June 2016
The cell biology of secondary cell wall biosynthesis Meents, Miranda J.; Watanabe, Yoichiro; Samuels, A. Lacey Annals of Botany, Vol. 121, Issue 6 https://doi.org/10.1093/aob/mcy005	journal	February 2018
Molecular and biotechnological aspects of xylanases Kulkarni, Neeta; Shendye, Abhay; Rao, Mala FEMS Microbiology Reviews, Vol. 23, Issue 4, p. 411-456 https://doi.org/10.1111/j.1574-6976.1999.tb00407.x	journal	July 1999
Imaging the Enzymatic Digestion of Bacterial Cellulose Ribbons Reveals the Endo Character of the Cellobiohydrolase Cel6A from Humicola insolens and Its Mode of Synergy with Cellobiohydrolase Cel7A Boisset, C.; Fraschini, C.; Schulein, M. Applied and Environmental Microbiology, Vol. 66, Issue 4 https://doi.org/10.1128/AEM.66.4.1444-1452.2000	journal	April 2000
Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis Arantes, Valdeir; Saddler, Jack N. Biotechnology for Biofuels, Vol. 3, Issue 1 https://doi.org/10.1186/1754-6834-3-4	journal	January 2010
Supplementation with xylanase and β-xylosidase to reduce xylo-oligomer and xylan inhibition of enzymatic hydrolysis of cellulose and pretreated corn stover Qing, Qing; Wyman, Charles E. Biotechnology for Biofuels, Vol. 4, Issue 1, Article No: 18 https://doi.org/10.1186/1754-6834-4-18	journal	June 2011
The enhancement of enzymatic hydrolysis of lignocellulosic substrates by the addition of accessory enzymes such as xylanase: is it an additive or synergistic effect? Hu, Jinguang; Arantes, Valdeir; Saddler, Jack N. Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-36	journal	January 2011
Xylan oligosaccharides and cellobiohydrolase I (TrCel7A) interaction and effect on activity Baumann, Martin J.; Borch, Kim; Westh, Peter Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-45	journal	January 2011
Interfacial molecular interactions of cellobiohydrolase Cel7A and its variants on cellulose Mudinoor, Akshata R.; Goodwin, Peter M.; Rao, Raghavendra U. Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-1649-7	journal	January 2020
Integrated multi-wavelength microscope combining TIRFM and IRM modalities for imaging cellulases and other processive enzymes Nong, Daguan; Haviland, Zachary K.; Kuntz, Kate Vasquez Biomedical Optics Express, Vol. 12, Issue 6 https://doi.org/10.1364/BOE.423798	journal	January 2021
Industrial-Scale Production and Applications of Bacterial Cellulose Zhong, Chunyan Frontiers in Bioengineering and Biotechnology, Vol. 8 https://doi.org/10.3389/fbioe.2020.605374	journal	December 2020
Pretreatment Affects Profits From Xylanase During Enzymatic Saccharification of Corn Stover Through Changing the Interaction Between Lignin and Xylanase Protein Feng, Xiaoting; Yao, Yini; Xu, Nuo Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.754593	journal	December 2021
Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls Crowe, Jacob D.; Hao, Pengchao; Pattathil, Sivakumar Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.737690	journal	September 2021
Bacterial Cellulose: Production, Characterization, and Application as Antimicrobial Agent Lahiri, Dibyajit; Nag, Moupriya; Dutta, Bandita International Journal of Molecular Sciences, Vol. 22, Issue 23 https://doi.org/10.3390/ijms222312984	journal	November 2021
The Nanofication and Functionalization of Bacterial Cellulose and Its Applications Choi, Soon Mo; Shin, Eun Joo Nanomaterials, Vol. 10, Issue 3 https://doi.org/10.3390/nano10030406	journal	February 2020

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