Insights into the action of phylogenetically diverse microbial expansins on the structure of cellulose microfibrils

Momeni, Majid Haddad; Zitting, Aleksi; Jäämuru, Vilma; Turunen, Rosaliina; Penttilä, Paavo; Buchko, Garry W.; Hiltunen, Salla; Maiorova, Natalia; Koivula, Anu; Sapkota, Janak; Marjamaa, Kaisa; Master, Emma R.

doi:10.1186/s13068-024-02500-w

Title: Insights into the action of phylogenetically diverse microbial expansins on the structure of cellulose microfibrils

Journal Article · 22 April 2024 · Biotechnology for Biofuels and Bioproducts

DOI: https://doi.org/10.1186/s13068-024-02500-w · OSTI ID:2341731

Momeni, Majid Haddad ^[1]; Zitting, Aleksi ^[1]; Jäämuru, Vilma ^[1]; Turunen, Rosaliina ^[1]; Penttilä, Paavo ^[1];

^[2]; Hiltunen, Salla ^[3]; Maiorova, Natalia ^[4]; Koivula, Anu ^[4]; Sapkota, Janak ^[3]; Marjamaa, Kaisa ^[4]; Master, Emma R. ^[5]

Aalto University, Otaniemi (Finland)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Washington State University, Pullman, WA (United States)
NE Research Center, UPM Pulp Research and Innovations, Lappeenranta (Finland)
VTT Technical Research Centre of Finland Ltd., Espoo (Finland)
Aalto University, Otaniemi (Finland); University of Toronto, ON (Canada)

Microbial expansins (EXLXs) are non-lytic proteins homologous to plant expansins involved in plant cell wall formation. Due to their non-lytic cell wall loosening properties and potential to disaggregate cellulosic structures, there is considerable interest in exploring the ability of microbial expansins (EXLX) to assist the processing of cellulosic biomass for broader biotechnological applications. Herein, EXLXs with different modular structure and from diverse phylogenetic origin were compared in terms of ability to bind cellulosic, xylosic, and chitinous substrates, to structurally modify cellulosic fibrils, and to boost enzymatic deconstruction of hardwood pulp. Five heterogeneously produced EXLXs (Clavibacter michiganensis; CmiEXLX2, Dickeya aquatica; DaqEXLX1, Xanthomonas sacchari; XsaEXLX1, Nothophytophthora sp.; NspEXLX1 and Phytophthora cactorum; PcaEXLX1) were shown to bind xylan and hardwood pulp at pH 5.5 and CmiEXLX2 (harboring a family-2 carbohydrate-binding module) also bound well to crystalline cellulose. Small-angle X-ray scattering revealed a 20–25% increase in interfibrillar distance between neighboring cellulose microfibrils following treatment with CmiEXLX2, DaqEXLX1, or NspEXLX1. Correspondingly, combining xylanase with CmiEXLX2 and DaqEXLX1 increased product yield from hardwood pulp by ~ 25%, while supplementing the TrAA9A LPMO from Trichoderma reesei with CmiEXLX2, DaqEXLX1, and NspEXLX1 increased total product yield by over 35%. This direct comparison of diverse EXLXs revealed consistent impacts on interfibrillar spacing of cellulose microfibers and performance of carbohydrate-active enzymes predicted to act on fiber surfaces. These findings uncover new possibilities to employ EXLXs in the creation of value-added materials from cellulosic biomass.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); European Union’s Horizon 2020; Academy of Finland; FinnCERES Materials Bioeconomy Ecosystem

Grant/Contract Number:: AC05-76RL01830; AC02-05CH11231

OSTI ID:: 2341731

Report Number(s):: PNNL-SA-187033

Journal Information:: Biotechnology for Biofuels and Bioproducts, Journal Name: Biotechnology for Biofuels and Bioproducts Journal Issue: 1 Vol. 17; ISSN 2731-3654

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (61)

Extraordinary μs–ms backbone dynamics in Arabidopsis thaliana peroxiredoxin Q Ådén, Jörgen; Wallgren, Marcus; Storm, Patrik Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1814, Issue 12 https://doi.org/10.1016/j.bbapap.2011.07.011	journal	December 2011
An NMR approach to structural proteomics Yee, A.; Chang, X.; Pineda-Lucena, A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 4 https://doi.org/10.1073/pnas.042684599	journal	February 2002
Oxidative modification of cellulosic fibres by lytic polysaccharide monooxygenase AA9A from Trichoderma reesei Marjamaa, Kaisa; Rahikainen, Jenni; Karjalainen, Marika Cellulose, Vol. 29, Issue 11 https://doi.org/10.1007/s10570-022-04648-w	journal	June 2022
Determination of protein secondary structure in solution by vacuum ultraviolet circular dichroism Brahms, S.; Brahms, J. Journal of Molecular Biology, Vol. 138, Issue 2 https://doi.org/10.1016/0022-2836(80)90282-X	journal	April 1980
Nuclear magnetic resonance observation and dynamics of specific amide protons in T4 lysozyme Griffey, Richard H.; Redfield, Alfred G.; Loomis, Ronald E. Biochemistry, Vol. 24, Issue 4 https://doi.org/10.1021/bi00325a001	journal	February 1985
Promotion of Efficient Saccharification of Crystalline Cellulose by Aspergillus fumigatus Swo1 Chen, Xin-ai; Ishida, Nobuhiro; Todaka, Nemuri Applied and Environmental Microbiology, Vol. 76, Issue 8 https://doi.org/10.1128/AEM.02499-09	journal	February 2010
Research advances in expansins and expansion-like proteins involved in lignocellulose degradation Liu, Xuewei; Ma, Yuanyuan; Zhang, Minhua Biotechnology Letters, Vol. 37, Issue 8 https://doi.org/10.1007/s10529-015-1842-0	journal	May 2015
Intrinsic Tryptophan Fluorescence in the Detection and Analysis of Proteins: A Focus on Förster Resonance Energy Transfer Techniques Ghisaidoobe, Amar; Chung, Sang International Journal of Molecular Sciences, Vol. 15, Issue 12 https://doi.org/10.3390/ijms151222518	journal	December 2014
Expansin Engineering Database: A navigation and classification tool for expansins and homologues Lohoff, Caroline; Buchholz, Patrick C. F.; Le Roes‐Hill, Marilize Proteins: Structure, Function, and Bioinformatics, Vol. 89, Issue 2 https://doi.org/10.1002/prot.26001	journal	September 2020
Plant Expansins in Bacteria and Fungi: Evolution by Horizontal Gene Transfer and Independent Domain Fusion Nikolaidis, Nikolas; Doran, Nicole; Cosgrove, Daniel J. Molecular Biology and Evolution, Vol. 31, Issue 2 https://doi.org/10.1093/molbev/mst206	journal	October 2013
How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis Jäger, Gernot; Girfoglio, Michele; Dollo, Florian Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-33	journal	January 2011
Swollenin from Trichoderma reesei exhibits hydrolytic activity against cellulosic substrates with features of both endoglucanases and cellobiohydrolases Andberg, Martina; Penttilä, Merja; Saloheimo, Markku Bioresource Technology, Vol. 181 https://doi.org/10.1016/j.biortech.2015.01.024	journal	April 2015
Biomechanical Weakening of Paper and Plant Cell Walls by Bacterial Expansins Cosgrove, Daniel J.; Hepler, Nathan K.; Wagner, Edward R. Carbohydrate-Protein Interactions https://doi.org/10.1007/978-1-0716-3151-5_5	book	May 2023
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Crystal structure and activities of EXPB1 (Zea m 1), a beta-expansin and group-1 pollen allergen from maize Yennawar, N. H.; Li, L. -C.; Dudzinski, D. M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 40 https://doi.org/10.1073/pnas.0605979103	journal	September 2006
Synergistic proteins for the enhanced enzymatic hydrolysis of cellulose by cellulase Kim, In Jung; Lee, Hee Jin; Choi, In-Geol Applied Microbiology and Biotechnology, Vol. 98, Issue 20 https://doi.org/10.1007/s00253-014-6001-3	journal	August 2014
Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization Kerff, F.; Amoroso, A.; Herman, R. Proceedings of the National Academy of Sciences, Vol. 105, Issue 44 https://doi.org/10.1073/pnas.0809382105	journal	October 2008
Interactive Tree Of Life (iTOL) v4: recent updates and new developments Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz239	journal	April 2019
Scission of Glucosidic Bonds by a Lentinus similis Lytic Polysaccharide Monooxygenases Is Strictly Dependent on H₂O₂ while the Oxidation of Saccharide Products Depends on O₂ Brander, Søren; Tokin, Radina; Ipsen, Johan Ø. ACS Catalysis, Vol. 11, Issue 22 https://doi.org/10.1021/acscatal.1c04248	journal	October 2021
MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization Katoh, Kazutaka; Rozewicki, John; Yamada, Kazunori D. Briefings in Bioinformatics, Vol. 20, Issue 4 https://doi.org/10.1093/bib/bbx108	journal	September 2017
Bacterial expansins and related proteins from the world of microbes Georgelis, Nikolaos; Nikolaidis, Nikolas; Cosgrove, Daniel J. Applied Microbiology and Biotechnology, Vol. 99, Issue 9 https://doi.org/10.1007/s00253-015-6534-0	journal	April 2015
Functional characterization of a bacterial expansin from Bacillus subtilis for enhanced enzymatic hydrolysis of cellulose Kim, Eun Sil; Lee, Hee Jin; Bang, Won-Gi Biotechnology and Bioengineering, Vol. 102, Issue 5 https://doi.org/10.1002/bit.22193	journal	April 2009
Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin Georgelis, N.; Yennawar, N. H.; Cosgrove, D. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 37 https://doi.org/10.1073/pnas.1213200109	journal	August 2012
Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions Greenfield, Norma J. Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.204	journal	December 2006
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls Wang, T.; Park, Y. B.; Caporini, M. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 41 https://doi.org/10.1073/pnas.1316290110	journal	September 2013
Interactions of Human Nucleotide Excision Repair Protein XPA with DNA and RPA70ΔC327: Chemical Shift Mapping and ¹⁵ N NMR Relaxation Studies ^† Buchko, Garry W.; Daughdrill, Gary W.; de Lorimier, Robert Biochemistry, Vol. 38, Issue 46 https://doi.org/10.1021/bi991755p	journal	November 1999
Real-time adsorption and action of expansin on cellulose Duan, Yuhao; Ma, Yuanyuan; Zhao, Xudong Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1318-2	journal	November 2018
Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials: A fungal expansin homologue Saloheimo, Markku; Paloheimo, Marja; Hakola, Satu European Journal of Biochemistry, Vol. 269, Issue 17 https://doi.org/10.1046/j.1432-1033.2002.03095.x	journal	August 2002
Use of substructure-specific carbohydrate binding modules to track changes in cellulose accessibility and surface morphology during the amorphogenesis step of enzymatic hydrolysis Gourlay, Keith; Arantes, Valdeir; Saddler, Jack N. Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-51	journal	January 2012
CSI 3.0: a web server for identifying secondary and super-secondary structure in proteins using NMR chemical shifts Hafsa, Noor E.; Arndt, David; Wishart, David S. Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv494	journal	May 2015
PcExl1 a Novel Acid Expansin-Like Protein from the Plant Pathogen Pectobacterium carotovorum, Binds Cell Walls Differently to BsEXLX1 Olarte-Lozano, Miguel; Mendoza-Nuñez, Mario A.; Pastor, Nina PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0095638	journal	April 2014
NGPhylogeny.fr: new generation phylogenetic services for non-specialists Lemoine, Frédéric; Correia, Damien; Lefort, Vincent Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz303	journal	April 2019
Microbial Expansins Cosgrove, Daniel J. Annual Review of Microbiology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-micro-090816-093315	journal	September 2017
Prevalent association with the bacterial cell envelope of prokaryotic expansins revealed by bioinformatics analysis de Sandozequi, Andrés; Salazar‐Cortés, Juan José; Tapia‐Vázquez, Irán Protein Science, Vol. 31, Issue 5 https://doi.org/10.1002/pro.4315	journal	April 2022
Colorimetric and fluorometric carbohydrate determination with p-hydroxybenzoic acid hydrazide Lever, M. Biochemical Medicine, Vol. 7, Issue 2 https://doi.org/10.1016/0006-2944(73)90083-5	journal	April 1973
I-TASSER server for protein 3D structure prediction Zhang, Yang BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-40	journal	January 2008
Understanding the structure and function of bacterial expansins: a prerequisite towards practical applications for the bioenergy and agricultural industries Martinez-Anaya, Claudia Microbial Biotechnology, Vol. 9, Issue 6 https://doi.org/10.1111/1751-7915.12377	journal	July 2016
Real-time adsorption and action of expansin on cellulose Duan, Yuhao; Ma, Yuanyuan; Zhao, Xudong figshare https://doi.org/10.6084/m9.figshare.c.4311299.v1	collection	January 2018
Loosenin, a novel protein with cellulose-disrupting activity from Bjerkandera adusta Quiroz-Castañeda, Rosa E.; Martínez-Anaya, Claudia; Cuervo-Soto, Laura I. Microbial Cell Factories, Vol. 10, Issue 1 https://doi.org/10.1186/1475-2859-10-8	journal	January 2011
The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp. sepedonicus plays a role in virulence and contains an expansin-like domain Laine, Marko J.; Haapalainen, Minna; Wahlroos, Tony Physiological and Molecular Plant Pathology, Vol. 57, Issue 5 https://doi.org/10.1006/pmpp.2000.0301	journal	November 2000
Structure-Function Analysis of the Bacterial Expansin EXLX1 Georgelis, Nikolaos; Tabuchi, Akira; Nikolaidis, Nikolas Journal of Biological Chemistry, Vol. 286, Issue 19 https://doi.org/10.1074/jbc.M111.225037	journal	March 2011
An expansin-like protein from Hahella chejuensis binds cellulose and enhances cellulase activity Lee, Hee Jin; Lee, Saeyoung; Ko, Hyeok-jin Molecules and Cells, Vol. 29, Issue 4 https://doi.org/10.1007/s10059-010-0033-z	journal	March 2010
Electrostatic analysis of bacterial expansins Pastor, Nina; Dávila, Sonia; Pérez‐Rueda, Ernesto Proteins: Structure, Function, and Bioinformatics, Vol. 83, Issue 2 https://doi.org/10.1002/prot.24718	journal	November 2014
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Sequence diversity and gene expression analyses of expansin-related proteins in the white-rot basidiomycete, Phanerochaete carnosa Suzuki, Hitoshi; Vuong, Thu V.; Gong, Yunchen Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.05.008	journal	November 2014
Binding characteristics and synergistic effects of bacterial expansins on cellulosic and hemicellulosic substrates Bunterngsook, Benjarat; Eurwilaichitr, Lily; Thamchaipenet, Arinthip Bioresource Technology, Vol. 176 https://doi.org/10.1016/j.biortech.2014.11.042	journal	January 2015
A structural fibrillation parameter from small angle X-ray scattering to quantify pulp refining Mao, Jia; Heck, Barbara; Abushammala, Hatem Cellulose, Vol. 26, Issue 7 https://doi.org/10.1007/s10570-019-02386-0	journal	March 2019
Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes Cosgrove, Daniel J. Journal of Experimental Botany, Vol. 67, Issue 2 https://doi.org/10.1093/jxb/erv511	journal	November 2015
Backbone chemical shift assignments for the SARS-CoV-2 non-structural protein Nsp9: intermediate (ms – μs) dynamics in the C-terminal helix at the dimer interface Buchko, Garry W.; Zhou, Mowei; Craig, Justin K. Biomolecular NMR Assignments, Vol. 15, Issue 1 https://doi.org/10.1007/s12104-020-09992-1	journal	January 2021
Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls Cosgrove, Daniel J. Planta, Vol. 177, Issue 1 https://doi.org/10.1007/BF00392162	journal	January 1989
Nomenclature for members of the expansin superfamily of genes and proteins Kende, Hans; Bradford, Kent; Brummell, David Plant Molecular Biology, Vol. 55, Issue 3 https://doi.org/10.1007/s11103-004-0158-6	journal	May 2004
Evaluation of swollenin from Trichoderma pseudokoningii as a potential synergistic factor in the enzymatic hydrolysis of cellulose with low cellulase loadings Zhou, Qingxin; Lv, Xinxing; Zhang, Xi World Journal of Microbiology and Biotechnology, Vol. 27, Issue 8 https://doi.org/10.1007/s11274-011-0650-5	journal	January 2011
Biochemical analysis of expansin-like proteins from microbes Georgelis, Nikolaos; Nikolaidis, Nikolas; Cosgrove, Daniel J. Carbohydrate Polymers, Vol. 100 https://doi.org/10.1016/j.carbpol.2013.04.094	journal	January 2014
Functional characterization of the native swollenin from Trichoderma reesei: study of its possible role as C1 factor of enzymatic lignocellulose conversion Eibinger, Manuel; Sigl, Karin; Sattelkow, Jürgen Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0590-2	journal	August 2016
Boosting enzymatic degradation of cellulose using a fungal expansin: Structural insight into the pretreatment mechanism Ding, Sunjia; Liu, Xiaoqing; Hakulinen, Nina Bioresource Technology, Vol. 358 https://doi.org/10.1016/j.biortech.2022.127434	journal	August 2022
Swollenin aids in the amorphogenesis step during the enzymatic hydrolysis of pretreated biomass Gourlay, Keith; Hu, Jinguang; Arantes, Valdeir Bioresource Technology, Vol. 142 https://doi.org/10.1016/j.biortech.2013.05.053	journal	August 2013
Loosening of plant cell walls by expansins Cosgrove, Daniel J. Nature, Vol. 407, Issue 6802 https://doi.org/10.1038/35030000	journal	September 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
The liquid fraction from hydrothermal pretreatment of wheat straw provides lytic polysaccharide monooxygenases with both electrons and H2O2 co-substrate Kont, Riin; Pihlajaniemi, Ville; Borisova, Anna S. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1578-5	journal	October 2019
Measuring the Biomechanical Loosening Action of Bacterial Expansins on Paper and Plant Cell Walls Cosgrove, Daniel J.; Hepler, Nathan K.; Wagner, Edward R. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-6899-2_12	book	January 2017

Similar Records

Bacterial expansins and related proteins from the world of microbes

Journal Article · 2015 · Applied Microbiology and Biotechnology · OSTI ID:1343258

Georgelis, Nikolaos; Nikolaidis, Nikolas; Cosgrove, Daniel J.

A Multiomic Approach to Understand How Pleurotus eryngii Transforms Non-Woody Lignocellulosic Material

Journal Article · 2021 · Journal of Fungi · OSTI ID:1785145

Peña, Ander; Babiker, Rashid; Chaduli, Delphine; +15 more

Loosenin-Like Proteins from Phanerochaete carnosa Impact Both Cellulose and Chitin Fiber Networks

Journal Article · 2023 · Applied and Environmental Microbiology · OSTI ID:1909472

Monschein, Mareike; Ioannou, Eleni; Koitto, Taru; +7 more

Related Subjects

09 BIOMASS FUELS
lignocellulose degradation
NMR spectroscopy
expansins
SAXS
WAXS
carbohydrate binding module

Title: Insights into the action of phylogenetically diverse microbial expansins on the structure of cellulose microfibrils

Citation Formats

References (61)

Similar Records

Related Subjects