Protective effects of non–catalytic proteins on endoglucanase activity at air and lignin interfaces

Almeida, Renata M. R. G.; Pimentel, Wagner R. O.; Santos‐Rocha, Martha S. R.; Buffo, Mariane M.; Farinas, Cristiane Sanchez; Ximenes, Eduardo A.; Ladisch, Michael R.

doi:10.1002/btpr.3134

Title: Protective effects of non–catalytic proteins on endoglucanase activity at air and lignin interfaces

Journal Article · Tue Apr 20 00:00:00 EDT 2021 · Biotechnology Progress

DOI:https://doi.org/10.1002/btpr.3134· OSTI ID:1994396

^[1];

^[2];

^[3];

^[4];

^[5];

^[5]

Federal University of Alagoas, Maceió (Brazil)
Federal Institute of Alagoas, Penado (Brazil)
Federal Univ. of Sao Carlos, Sao Paulo (Brazil)
Federal Univ. of Sao Carlos, Sao Paulo (Brazil); Embrapa Instrumentação, São Carlos, São Paulo (Brazil)
Purdue Univ., West Lafayette, IN (United States)

The manner in which added non-catalytic proteins during enzymatic hydrolysis of lignocellulosic substrates enhances hydrolysis mechanisms is not completely understood. Prior research has indicated that a reduction in the non-specific adsorption of enzymes on lignin, and deactivation of enzymes exposed to air–liquid interface provide rationale. This work investigated root causes including effects of the air–liquid interface on non-catalytic proteins, and effects of lignin on endoglucanase. Three different experimental designs and three variables (air–liquid interfacial area, the types of lignin (acid or enzymatic lignin), and the presence of non-enzymatic protein (bovine serum albumin [BSA] or soy proteins ) were used. The results showed that acid isolated lignin adsorbed almost all endoglucanase activity initially present in supernatant, independent of air interface conditions (25 or 250 ml flasks) with the presence of BSA preventing this effect. Endoglucanase lost 30%–50% of its activity due to an air–liquid interface in the presence of lignin while addition of non-enzymatic protein helped to preserve this enzyme's activity. Langmuir and Freundlich models applied to experimental data indicated that the adsorption increases with increasing temperature for both endoglucanase and BSA. Adsorption of the enzyme and protein were endothermic with an increase in entropy. Finally, these results, combined, show that hydrophobicity plays a strong role in the adsorption of both endoglucanase and BSA on lignin.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Purdue Univ., West Lafayette, IN (United States)

Sponsoring Organization:: USDOE; National Council for Scientific and Technological Development, Brazil (CNPq); São Paulo State Research Foundation, Brazil (FAPESP)

Grant/Contract Number:: EE0008256; 206641/2017-6; 2016/10636-8

OSTI ID:: 1994396

Journal Information:: Biotechnology Progress, Vol. 37, Issue 4; ISSN 8756-7938

Publisher:: Society for Biological EngineeringCopyright Statement

Country of Publication:: United States

Language:: English

References (50)

Effect of temperature on lignin-derived inhibition studied with three structurally different cellobiohydrolases Rahikainen, Jenni Liisa; Moilanen, Ulla; Nurmi-Rantala, Susanna Bioresource Technology, Vol. 146 https://doi.org/10.1016/j.biortech.2013.07.069	journal	October 2013
Addition of Soybean Protein Improves Saccharification and Ethanol Production from Hydrothermally Pretreated Sugarcane Bagasse Florencio, Camila; Badino, Alberto C.; Farinas, Cristiane S. BioEnergy Research, Vol. 12, Issue 1 https://doi.org/10.1007/s12155-018-9956-6	journal	January 2019
Dye removal from wastewater using activated carbon developed from sawdust: adsorption equilibrium and kinetics Malik, P. K. Journal of Hazardous Materials, Vol. 113, Issue 1-3 https://doi.org/10.1016/j.jhazmat.2004.05.022	journal	September 2004
Combined product and substrate inhibition equation for cellobiase Hong, Juan; Ladisch, Michael R.; Gong, Chen-shung Biotechnology and Bioengineering, Vol. 23, Issue 12 https://doi.org/10.1002/bit.260231212	journal	December 1981
Adsorption of Cellulase on Cellulolytic Enzyme Lignin from Lodgepole Pine Tu, Maobing; Pan, Xuejun; Saddler, Jack N. Journal of Agricultural and Food Chemistry, Vol. 57, Issue 17 https://doi.org/10.1021/jf901031m	journal	September 2009
Evaluation of the effects of isolated lignin on enzymatic hydrolysis of cellulose Zhang, Hongdan; Wu, Shubin; Xie, Jun Enzyme and Microbial Technology, Vol. 101 https://doi.org/10.1016/j.enzmictec.2017.03.001	journal	June 2017
Severity factor coefficients for subcritical liquid hot water pretreatment of hardwood chips: Severity Factor for Liquid Hot Water Pretreatment Kim, Youngmi; Kreke, Thomas; Mosier, Nathan S. Biotechnology and Bioengineering, Vol. 111, Issue 2 https://doi.org/10.1002/bit.25009	journal	August 2013
Effects of dilute acid and flowthrough pretreatments and BSA supplementation on enzymatic deconstruction of poplar by cellulase and xylanase Bhagia, Samarthya; Kumar, Rajeev; Wyman, Charles E. Carbohydrate Polymers, Vol. 157 https://doi.org/10.1016/j.carbpol.2016.11.085	journal	February 2017
Adsorption and desorption of cellulases on/from lignin-rich residues from corn stover Hao, Xixun; Li, Yanfei; Wang, Jinye Industrial Crops and Products, Vol. 139 https://doi.org/10.1016/j.indcrop.2019.111559	journal	November 2019
Investigation of adsorption kinetics and isotherm of cellulase and β-glucosidase on lignocellulosic substrates Zheng, Yi; Zhang, Ruihong; Pan, Zhongli Biomass and Bioenergy, Vol. 91 https://doi.org/10.1016/j.biombioe.2016.04.014	journal	August 2016
Alternative Low-Cost Additives to Improve the Saccharification of Lignocellulosic Biomass Brondi, Mariana G.; Vasconcellos, Vanessa M.; Giordano, Roberto C. Applied Biochemistry and Biotechnology, Vol. 187, Issue 2 https://doi.org/10.1007/s12010-018-2834-z	journal	July 2018
Some consideration on the Langmuir isotherm equation Liu, Yu Colloids and Surfaces A: Physicochemical and Engineering Aspects, Vol. 274, Issue 1-3 https://doi.org/10.1016/j.colsurfa.2005.08.029	journal	February 2006
BSA treatment to enhance enzymatic hydrolysis of cellulose in lignin containing substrates Yang, Bin; Wyman, Charles E. Biotechnology and Bioengineering, Vol. 94, Issue 4 https://doi.org/10.1002/bit.20750	journal	January 2006
Kinetic dynamics in heterogeneous enzymatic hydrolysis of cellulose: an overview, an experimental study and mathematical modelling Gan, Q.; Allen, S. J.; Taylor, G. Process Biochemistry, Vol. 38, Issue 7 https://doi.org/10.1016/S0032-9592(02)00220-0	journal	February 2003
Temperature dependent cellulase adsorption on lignin from sugarcane bagasse Zanchetta, Ariane; dos Santos, Antonio Carlos Freitas; Ximenes, Eduardo Bioresource Technology, Vol. 252 https://doi.org/10.1016/j.biortech.2017.12.061	journal	March 2018
Inhibition of cellulase, xylanase and β-glucosidase activities by softwood lignin preparations Berlin, Alex; Balakshin, Mikhail; Gilkes, Neil Journal of Biotechnology, Vol. 125, Issue 2, p. 198-209 https://doi.org/10.1016/j.jbiotec.2006.02.021	journal	September 2006
Deactivation of Cellulase at the Air-Liquid Interface Is the Main Cause of Incomplete Cellulose Conversion at Low Enzyme Loadings Bhagia, Samarthya; Dhir, Rachna; Kumar, Rajeev Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-19848-3	journal	January 2018
Performance targets defined by retro-techno-economic analysis for the use of soybean protein as saccharification additive in an integrated biorefinery Brondi, Mariana G.; Elias, Andrew M.; Furlan, Felipe F. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-64316-6	journal	April 2020
Effect of surfactants on cellulose hydrolysis Helle, Steve S.; Duff, Sheldon J. B.; Cooper, David G. Biotechnology and Bioengineering, Vol. 42, Issue 5 https://doi.org/10.1002/bit.260420509	journal	August 1993
Inhibitory effects of lignin on enzymatic hydrolysis: The role of lignin chemistry and molecular weight Li, Xiang; Li, Mi; Pu, Yunqiao Renewable Energy, Vol. 123 https://doi.org/10.1016/j.renene.2018.02.079	journal	August 2018
Biosorption kinetics and isotherm studies of Acid Red 57 by dried Cephalosporium aphidicola cells from aqueous solutions Kiran, Ismail; Akar, Tamer; Ozcan, A. Safa Biochemical Engineering Journal, Vol. 31, Issue 3 https://doi.org/10.1016/j.bej.2006.07.008	journal	October 2006
Evaluation of the action of Tween 20 non-ionic surfactant during enzymatic hydrolysis of lignocellulose: Pretreatment, hydrolysis conditions and lignin structure Chen, Yu-An; Zhou, Yan; Qin, Yanlin Bioresource Technology, Vol. 269 https://doi.org/10.1016/j.biortech.2018.08.119	journal	December 2018
Temperature and pH influence adsorption of cellobiohydrolase onto lignin by changing the protein properties Lu, Xianqin; Wang, Can; Li, Xuezhi Bioresource Technology, Vol. 245 https://doi.org/10.1016/j.biortech.2017.08.139	journal	December 2017
Measurement of cellulase activities Ghose, T. K. Pure and Applied Chemistry, Vol. 59, Issue 2 https://doi.org/10.1351/pac198759020257	journal	January 1987
The isolation, characterization and effect of lignin isolated from steam pretreated Douglas-fir on the enzymatic hydrolysis of cellulose Nakagame, Seiji; Chandra, Richard P.; Kadla, John F. Bioresource Technology, Vol. 102, Issue 6 https://doi.org/10.1016/j.biortech.2010.12.082	journal	March 2011
Surface deactivation of cellulase and its prevention Kim, M. H.; Lee, S. B.; Ryu, Dewey D. Y. Enzyme and Microbial Technology, Vol. 4, Issue 2 https://doi.org/10.1016/0141-0229(82)90090-4	journal	March 1982
Nonionic surfactants enhanced enzymatic hydrolysis of cellulose by reducing cellulase deactivation caused by shear force and air-liquid interface Lou, Hongming; Zeng, Meijun; Hu, Qiaoyan Bioresource Technology, Vol. 249 https://doi.org/10.1016/j.biortech.2017.07.066	journal	February 2018
Soybean protein as a cost-effective lignin-blocking additive for the saccharification of sugarcane bagasse Florencio, Camila; Badino, Alberto C.; Farinas, Cristiane S. Bioresource Technology, Vol. 221 https://doi.org/10.1016/j.biortech.2016.09.039	journal	December 2016
Inhibition of cellulases by phenols Ximenes, Eduardo; Kim, Youngmi; Mosier, Nathan Enzyme and Microbial Technology, Vol. 46, Issue 3-4, p. 170-176 https://doi.org/10.1016/j.enzmictec.2009.11.001	journal	March 2010
Adsorption Mode of Exo- and Endo-Cellulases from Irpex lacteus (Polyporus tulipiferae) on Cellulose with Different Crystallinities Hoshino, Eiichi; Kanda, Takahisa; Sasaki, Yasushi The Journal of Biochemistry, Vol. 111, Issue 5 https://doi.org/10.1093/oxfordjournals.jbchem.a123804	journal	May 1992
Fractionation of cellulase and fermentation inhibitors from steam pretreated mixed hardwood Kim, Youngmi; Kreke, Thomas; Hendrickson, Rick Bioresource Technology, Vol. 135 https://doi.org/10.1016/j.biortech.2012.10.130	journal	May 2013
786. Studies in adsorption. Part XI. A system of classification of solution adsorption isotherms, and its use in diagnosis of adsorption mechanisms and in measurement of specific surface areas of solids Giles, C. H.; MacEwan, T. H.; Nakhwa, S. N. Journal of the Chemical Society (Resumed) https://doi.org/10.1039/jr9600003973	journal	January 1960
The lignin present in steam pretreated softwood binds enzymes and limits cellulose accessibility Kumar, Linoj; Arantes, Valdeir; Chandra, Richard Bioresource Technology, Vol. 103, Issue 1 https://doi.org/10.1016/j.biortech.2011.09.091	journal	January 2012
Effect of using a nitrogen atmosphere on enzyme hydrolysis at high corn stover loadings in an agitated reactor Santos, Antonio Carlos Freitas; Ximenes, Eduardo; Thompson, David Biotechnology Progress, Vol. 36, Issue 6 https://doi.org/10.1002/btpr.3059	journal	August 2020
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar Miller, G. L. Analytical Chemistry, Vol. 31, Issue 3 https://doi.org/10.1021/ac60147a030	journal	March 1959
Effect of liquid hot water pretreatment severity on properties of hardwood lignin and enzymatic hydrolysis of cellulose: Lignin Effect on Enzyme Hydrolysis of Cellulose Ko, Ja Kyong; Kim, Youngmi; Ximenes, Eduardo Biotechnology and Bioengineering, Vol. 112, Issue 2 https://doi.org/10.1002/bit.25349	journal	October 2014
Adsorption and mechanism of cellulase enzymes onto lignin isolated from corn stover pretreated with liquid hot water Lu, Xianqin; Zheng, Xiaoju; Li, Xuezhi Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0531-0	journal	June 2016
Determination of adsorption and speciation of chromium species by saltbush (Atriplex canescens) biomass using a combination of XAS and ICP–OES Sawalha, M. F.; Gardea-Torresdey, J. L.; Parsons, J. G. Microchemical Journal, Vol. 81, Issue 1 https://doi.org/10.1016/j.microc.2005.01.008	journal	August 2005
Hydrolysis-determining substrate characteristics in liquid hot water pretreated hardwood: Hydrolysis-Determining Substrate Characteristics Kim, Youngmi; Kreke, Thomas; Ko, Ja Kyong Biotechnology and Bioengineering, Vol. 112, Issue 4 https://doi.org/10.1002/bit.25465	journal	January 2015
Structures and Stabilities of Adsorbed Proteins Haynes, Charles A.; Norde, Willem Journal of Colloid and Interface Science, Vol. 169, Issue 2 https://doi.org/10.1006/jcis.1995.1039	journal	February 1995
Lignin–Enzyme Interactions in the Hydrolysis of Lignocellulosic Biomass dos Santos, Antonio Carlos; Ximenes, Eduardo; Kim, Youngmi Trends in Biotechnology, Vol. 37, Issue 5 https://doi.org/10.1016/j.tibtech.2018.10.010	journal	May 2019
Enzymatic hydrolysis of lignocellulosic biomass from low to high solids loading Chen, Hong-Zhang; Liu, Zhi-Hua Engineering in Life Sciences, Vol. 17, Issue 5 https://doi.org/10.1002/elsc.201600102	journal	December 2016
Single-step unimolecular non-first-order enzyme deactivation kinetics Sadana, Ajit; Henley, James P. Biotechnology and Bioengineering, Vol. 30, Issue 6 https://doi.org/10.1002/bit.260300604	journal	October 1987
Influence of temperature on the kinetics of adsorption and desorption of clavulanic acid by ionic exchange Barboza, Marlei; Almeida, Renata M. R. G.; Hokka, Carlos. O. Biochemical Engineering Journal, Vol. 14, Issue 1 https://doi.org/10.1016/S1369-703X(02)00103-1	journal	April 2003
Deactivation of cellulases by phenols Ximenes, Eduardo; Kim, Youngmi; Mosier, Nathan Enzyme and Microbial Technology, Vol. 48, Issue 1 https://doi.org/10.1016/j.enzmictec.2010.09.006	journal	January 2011
Effect of poly(ethylene glycol) on enzymatic hydrolysis and adsorption of cellulase enzymes to pretreated lignocellulose Börjesson, Johan; Engqvist, Martin; Sipos, Bálint Enzyme and Microbial Technology, Vol. 41, Issue 1-2 https://doi.org/10.1016/j.enzmictec.2007.01.003	journal	July 2007
Effect of phenolic compounds from pretreated sugarcane bagasse on cellulolytic and hemicellulolytic activities Michelin, Michele; Ximenes, Eduardo; de Lourdes Teixeira de Moraes Polizeli, Maria Bioresource Technology, Vol. 199 https://doi.org/10.1016/j.biortech.2015.08.120	journal	January 2016
Benefits from Tween during enzymic hydrolysis of corn stover Kaar, William E.; Holtzapple, Mark T. Biotechnology and Bioengineering, Vol. 59, Issue 4 https://doi.org/10.1002/(SICI)1097-0290(19980820)59:4<419::AID-BIT4>3.0.CO;2-J	journal	August 1998
Adsorption of enzyme onto lignins of liquid hot water pretreated hardwoods: Enzyme Adsorption by Lignin in Hardwood Ko, Ja Kyong; Ximenes, Eduardo; Kim, Youngmi Biotechnology and Bioengineering, Vol. 112, Issue 3 https://doi.org/10.1002/bit.25359	journal	September 2014
Cellulase adsorption on lignin: A roadblock for economic hydrolysis of biomass Saini, Jitendra Kumar; Patel, Anil Kumar; Adsul, Mukund Renewable Energy, Vol. 98 https://doi.org/10.1016/j.renene.2016.03.089	journal	December 2016

Similar Records

Deactivation of Cellulase at the Air-Liquid Interface Is the Main Cause of Incomplete Cellulose Conversion at Low Enzyme Loadings

Journal Article · Mon Jan 22 00:00:00 EST 2018 · Scientific Reports · OSTI ID:1994396

Bhagia, Samarthya; Dhir, Rachna; Kumar, Rajeev; +1 more

Alternative Low-Cost Additives to Improve the Saccharification of Lignocellulosic Biomass

Journal Article · Fri Feb 15 00:00:00 EST 2019 · Applied Biochemistry and Biotechnology · OSTI ID:1994396

Impact of protein blocking on enzymatic saccharification of bagasse from sugarcane clones

Journal Article · Thu Mar 21 00:00:00 EDT 2019 · Biotechnology and Bioengineering · OSTI ID:1994396

Ázar, Rafaela I. S. Ladeira; Morgan, Túlio; Barbosa, Márcio H. P.; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
bovine serum albumin
cellulases
interfacial area
non-productive adsorption
soybean protein

Title: Protective effects of non–catalytic proteins on endoglucanase activity at air and lignin interfaces

Citation Formats

References (50)

Similar Records

Related Subjects