Use of Nanostructure-Initiator Mass Spectrometry to Deduce Selectivity of Reaction in Glycoside Hydrolases

Deng, Kai; Takasuka, Taichi E.; Bianchetti, Christopher M.; Bergeman, Lai F.; Adams, Paul D.; Northen, Trent R.; Fox, Brian G.

doi:10.3389/fbioe.2015.00165

Title: Use of Nanostructure-Initiator Mass Spectrometry to Deduce Selectivity of Reaction in Glycoside Hydrolases

Journal Article · 26 October 2015 · Frontiers in Bioengineering and Biotechnology

DOI: https://doi.org/10.3389/fbioe.2015.00165 · OSTI ID:1904711

Deng, Kai ^[1]; Takasuka, Taichi E. ^[2]; Bianchetti, Christopher M. ^[3]; Bergeman, Lai F. ^[2]; Adams, Paul D. ^[4]; Northen, Trent R. ^[4]; Fox, Brian G. ^[5]

Joint BioEnergy Institute (JBEI), Emeryville, CA (United States); Sandia National Laboratory (SNL-CA), Livermore, CA (United States); Univ. of Wisconsin, Madison, WI (United States)
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Oshkosh, WI (United States)
Joint BioEnergy Institute (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); University of Wisconsin, Madison, WI (United States)

Chemically synthesized nanostructure-initiator mass spectrometry (NIMS) probes derivatized with tetrasaccharides were used to study the reactivity of representative Clostridium thermocellum β-glucosidase, endoglucanases, and cellobiohydrolase. Diagnostic patterns for reactions of these different classes of enzymes were observed. Results show sequential removal of glucose by the β-glucosidase and a progressive increase in specificity of reaction from endoglucanases to cellobiohydrolase. Time-dependent reactions of these polysaccharide-selective enzymes were modeled by numerical integration, which provides a quantitative basis to make functional distinctions among a continuum of naturally evolved catalytic properties. Consequently, our method, which combines automated protein translation with high-sensitivity and time-dependent detection of multiple products, provides a new approach to annotate glycoside hydrolase phylogenetic trees with functional measurements.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Sandia National Laboratories (SNL-CA), Livermore, CA (United States); University of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; FC02-07ER64494

OSTI ID:: 1904711

Journal Information:: Frontiers in Bioengineering and Biotechnology, Journal Name: Frontiers in Bioengineering and Biotechnology Vol. 3; ISSN 2296-4185

Publisher:: Frontiers Media S.A.Copyright Statement

Country of Publication:: United States

Language:: English

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Flexi Vector Cloning Blommel, Paul G.; Martin, Peter A.; Seder, Kory D. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-196-3_4	book	January 2009
Cell-Free Translation of Biofuel Enzymes Takasuka, Taichi E.; Walker, Johnnie A.; Bergeman, Lai F. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-782-2_5	book	December 2013
Versatile synthesis of probes for high-throughput enzyme activity screening de Rond, Tristan; Peralta-Yahya, Pamela; Cheng, Xiaoliang Analytical and Bioanalytical Chemistry, Vol. 405, Issue 14 https://doi.org/10.1007/s00216-013-6888-z	journal	April 2013
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Towards Fully Automated Structure-based Function Prediction in Structural Genomics: A Case Study Watson, James D.; Sanderson, Steve; Ezersky, Alexandra Journal of Molecular Biology, Vol. 367, Issue 5 https://doi.org/10.1016/j.jmb.2007.01.063	journal	April 2007
Robotic large-scale application of wheat cell-free translation to structural studies including membrane proteins Beebe, Emily T.; Makino, Shin-ichi; Nozawa, Akira New Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1016/j.nbt.2010.07.003	journal	April 2011
Wheat germ cell-free protein production system for post-genomic research Madono, Masaki; Sawasaki, Tatsuya; Morishita, Ryo New Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1016/j.nbt.2010.08.009	journal	April 2011
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Identification of Two Functionally Different Classes of Exocellulases ^† Barr, Brian K.; Hsieh, Yin-Liang; Ganem, Bruce Biochemistry, Vol. 35, Issue 2 https://doi.org/10.1021/bi9520388	journal	January 1996
Rapid Kinetic Characterization of Glycosyl Hydrolases Based on Oxime Derivatization and Nanostructure-Initiator Mass Spectrometry (NIMS) Deng, Kai; Takasuka, Taichi E.; Heins, Richard ACS Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1021/cb5000289	journal	May 2014
Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry Heins, Richard A.; Cheng, Xiaoliang; Nath, Sangeeta ACS Chemical Biology, Vol. 9, Issue 9 https://doi.org/10.1021/cb500244v	journal	July 2014
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Coordinating the impact of structural genomics on the human α-helical transmembrane proteome Pieper, Ursula; Schlessinger, Avner; Kloppmann, Edda Nature Structural & Molecular Biology, Vol. 20, Issue 2 https://doi.org/10.1038/nsmb.2508	journal	February 2013
A nanostructure-initiator mass spectrometry-based enzyme activity assay Northen, T. R.; Lee, J.-C.; Hoang, L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 10, p. 3678-3683 https://doi.org/10.1073/pnas.0712332105	journal	March 2008
Active Site and Laminarin Binding in Glycoside Hydrolase Family 55 Bianchetti, Christopher M.; Takasuka, Taichi E.; Deutsch, Sam Journal of Biological Chemistry, Vol. 290, Issue 19 https://doi.org/10.1074/jbc.m114.623579	journal	March 2015
A Simplex Method for Function Minimization Nelder, J. A.; Mead, R. The Computer Journal, Vol. 7, Issue 4 https://doi.org/10.1093/comjnl/7.4.308	journal	January 1965
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
Fine Substrate Specificities of Four Exo-Type Cellulases Produced by Aspergillus niger, Trichoderma reesei, and Irpex lacteus on (1->3),(1->4)- -D-Glucans and Xyloglucan Amano, Y.; Shiroishi, M.; Nisizawa, K. Journal of Biochemistry, Vol. 120, Issue 6 https://doi.org/10.1093/oxfordjournals.jbchem.a021531	journal	December 1996
Gene sequence and properties of Cell, a family E endoglucanase from Clostridium thermocellum Hazlewood,, G. P.; Davidson, K.; Laurie, J. I. Journal of General Microbiology, Vol. 139, Issue 2 https://doi.org/10.1099/00221287-139-2-307	journal	February 1993
Cell-free protein synthesis and substrate specificity of full-length endoglucanase CelJ (Cel9D-Cel44A), the largest multi-enzyme subunit of theClostridium thermocellumcellulosome Hirano, Nobutaka; Hasegawa, Hiroki; Nihei, Satoshi FEMS Microbiology Letters, Vol. 344, Issue 1 https://doi.org/10.1111/1574-6968.12149	journal	April 2013
Structure of the beta-glucosidase gene bglA of Clostridium thermocellum. Sequence analysis reveals a superfamily of cellulases and beta-glycosidases including human lactase/phlorizin hydrolase Grabnitz, Folke; Seiss, Monika; Rucknagel, Karl P. European Journal of Biochemistry, Vol. 200, Issue 2 https://doi.org/10.1111/j.1432-1033.1991.tb16186.x	journal	September 1991
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Stoichiometric Assembly of the Cellulosome Generates Maximum Synergy for the Degradation of Crystalline Cellulose, as Revealed by In Vitro Reconstitution of the Clostridium thermocellum Cellulosome Hirano, Katsuaki; Nihei, Satoshi; Hasegawa, Hiroki Applied and Environmental Microbiology, Vol. 81, Issue 14 https://doi.org/10.1128/aem.00772-15	journal	July 2015
Global Gene Expression Patterns in Clostridium thermocellum as Determined by Microarray Analysis of Chemostat Cultures on Cellulose or Cellobiose Riederer, Allison; Takasuka, Taichi E.; Makino, Shin-ichi Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/aem.02008-10	journal	December 2010
Complete Genome Sequence of the Cellulolytic Thermophile Clostridium thermocellum DSM1313 Feinberg, L.; Foden, J.; Barrett, T. Journal of Bacteriology, Vol. 193, Issue 11, p. 2906-2907 https://doi.org/10.1128/jb.00322-11	journal	April 2011
Global View of the Clostridium thermocellum Cellulosome Revealed by Quantitative Proteomic Analysis Gold, N. D.; Martin, V. J. J. Journal of Bacteriology, Vol. 189, Issue 19 https://doi.org/10.1128/jb.00882-07	journal	July 2007
Cloning and Sequence Analysis of a New Cellulase Gene Encoding CelK, a Major Cellulosome Component of Clostridium thermocellum: Evidence for Gene Duplication and Recombination Kataeva, Irina; Li, Xin-Liang; Chen, Huizhong Journal of Bacteriology, Vol. 181, Issue 17 https://doi.org/10.1128/jb.181.17.5288-5295.1999	journal	September 1999
Cellulosomes: Highly Efficient Nanomachines Designed to Deconstruct Plant Cell Wall Complex Carbohydrates Fontes, Carlos M. G. A.; Gilbert, Harry J. Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev-biochem-091208-085603	journal	June 2010
Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation Raman, Babu; McKeown, Catherine K; Rodriguez, Miguel BMC Microbiology, Vol. 11, Issue 1, Article No. 134 https://doi.org/10.1186/1471-2180-11-134	journal	January 2011
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Encoding substrates with mass tags to resolve stereospecific reactions using Nimzyme: Encoding substrates with mass tags using Nimzyme Deng, Kai; George, Kevin W.; Reindl, Wolfgang Rapid Communications in Mass Spectrometry, Vol. 26, Issue 6 https://doi.org/10.1002/rcm.6134	journal	February 2012
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Cell-Free Protein Synthesis for Functional and Structural Studies Makino, Shin-ichi; Beebe, Emily T.; Markley, John L. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-691-7_11	book	October 2013
Cell-Free Translation of Biofuel Enzymes Takasuka, Taichi E.; Walker, Johnnie A.; Bergeman, Lai F. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-782-2_5	book	December 2013
Versatile synthesis of probes for high-throughput enzyme activity screening de Rond, Tristan; Peralta-Yahya, Pamela; Cheng, Xiaoliang Analytical and Bioanalytical Chemistry, Vol. 405, Issue 14 https://doi.org/10.1007/s00216-013-6888-z	journal	April 2013
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Structural genomics is the largest contributor of novel structural leverage Nair, Rajesh; Liu, Jinfeng; Soong, Ta-Tsen Journal of Structural and Functional Genomics, Vol. 10, Issue 2 https://doi.org/10.1007/s10969-008-9055-6	journal	February 2009
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Expression platforms for producing eukaryotic proteins: a comparison of E. coli cell-based and wheat germ cell-free synthesis, affinity and solubility tags, and cloning strategies Aceti, David J.; Bingman, Craig A.; Wrobel, Russell L. Journal of Structural and Functional Genomics, Vol. 16, Issue 2 https://doi.org/10.1007/s10969-015-9198-1	journal	April 2015
Construction and evaluation of a Clostridium thermocellum ATCC 27405 whole-genome oligonucleotide microarray Brown, Steven D.; Raman, Babu; McKeown, Catherine K. Applied Biochemistry and Biotechnology, Vol. 137-140, Issue 1-12 https://doi.org/10.1007/s12010-007-9087-6	journal	April 2007
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Structural and sequence-based classification of glycoside hydrolases Henrissat, Bernard; Davies, Gideon Current Opinion in Structural Biology, Vol. 7, Issue 5, p. 637-644 https://doi.org/10.1016/S0959-440X(97)80072-3	journal	October 1997
The crystal structure of endoglucanase CelA, a family 8 glycosyl hydrolase from Clostridium thermocellum Alzari, Pedro M.; ne Souchon, Hélè; Dominguez, Roberto Structure, Vol. 4, Issue 3 https://doi.org/10.1016/S0969-2126(96)00031-7	journal	March 1996
Modeling cellulase kinetics on lignocellulosic substrates Bansal, Prabuddha; Hall, Mélanie; Realff, Matthew J. Biotechnology Advances, Vol. 27, Issue 6 https://doi.org/10.1016/j.biotechadv.2009.06.005	journal	November 2009
A biophysical perspective on the cellulosome: new opportunities for biomass conversion Ding, Shi-You; Xu, Qi; Crowley, Michael Current Opinion in Biotechnology, Vol. 19, Issue 3 https://doi.org/10.1016/j.copbio.2008.04.008	journal	June 2008
A major new component in the cellulosome of Clostridium thermocellum is a processive endo-Î²-1,4-glucanase producing cellotetraose Zverlov, Vladimir V.; Schantz, Nikolaus; Schwarz, Wolfgang H. FEMS Microbiology Letters, Vol. 249, Issue 2 https://doi.org/10.1016/j.femsle.2005.06.037	journal	August 2005
Towards Fully Automated Structure-based Function Prediction in Structural Genomics: A Case Study Watson, James D.; Sanderson, Steve; Ezersky, Alexandra Journal of Molecular Biology, Vol. 367, Issue 5 https://doi.org/10.1016/j.jmb.2007.01.063	journal	April 2007
Robotic large-scale application of wheat cell-free translation to structural studies including membrane proteins Beebe, Emily T.; Makino, Shin-ichi; Nozawa, Akira New Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1016/j.nbt.2010.07.003	journal	April 2011
Wheat germ cell-free protein production system for post-genomic research Madono, Masaki; Sawasaki, Tatsuya; Morishita, Ryo New Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1016/j.nbt.2010.08.009	journal	April 2011
Insights into cellulosome assembly and dynamics: from dissection to reconstruction of the supramolecular enzyme complex Smith, Steven P.; Bayer, Edward A. Current Opinion in Structural Biology, Vol. 23, Issue 5 https://doi.org/10.1016/j.sbi.2013.09.002	journal	October 2013
Partition analysis and concept of net rate constants as tools in enzyme kinetics Cleland, W. W. Biochemistry, Vol. 14, Issue 14 https://doi.org/10.1021/bi00685a029	journal	July 1975
The Enzyme Function Initiative Gerlt, John A.; Allen, Karen N.; Almo, Steven C. Biochemistry, Vol. 50, Issue 46 https://doi.org/10.1021/bi201312u	journal	November 2011
Identification of Two Functionally Different Classes of Exocellulases ^† Barr, Brian K.; Hsieh, Yin-Liang; Ganem, Bruce Biochemistry, Vol. 35, Issue 2 https://doi.org/10.1021/bi9520388	journal	January 1996
Rapid Kinetic Characterization of Glycosyl Hydrolases Based on Oxime Derivatization and Nanostructure-Initiator Mass Spectrometry (NIMS) Deng, Kai; Takasuka, Taichi E.; Heins, Richard ACS Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1021/cb5000289	journal	May 2014
Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry Heins, Richard A.; Cheng, Xiaoliang; Nath, Sangeeta ACS Chemical Biology, Vol. 9, Issue 9 https://doi.org/10.1021/cb500244v	journal	July 2014
Structural genomics: from genes to structures with valuable materials and many questions in between Fox, Brian G.; Goulding, Celia; Malkowski, Michael G. Nature Methods, Vol. 5, Issue 2 https://doi.org/10.1038/nmeth0208-129	journal	February 2008
Coordinating the impact of structural genomics on the human α-helical transmembrane proteome Pieper, Ursula; Schlessinger, Avner; Kloppmann, Edda Nature Structural & Molecular Biology, Vol. 20, Issue 2 https://doi.org/10.1038/nsmb.2508	journal	February 2013
A nanostructure-initiator mass spectrometry-based enzyme activity assay Northen, T. R.; Lee, J.-C.; Hoang, L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 10, p. 3678-3683 https://doi.org/10.1073/pnas.0712332105	journal	March 2008
Active Site and Laminarin Binding in Glycoside Hydrolase Family 55 Bianchetti, Christopher M.; Takasuka, Taichi E.; Deutsch, Sam Journal of Biological Chemistry, Vol. 290, Issue 19 https://doi.org/10.1074/jbc.M114.623579	journal	March 2015
A Simplex Method for Function Minimization Nelder, J. A.; Mead, R. The Computer Journal, Vol. 7, Issue 4 https://doi.org/10.1093/comjnl/7.4.308	journal	January 1965
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
Fine Substrate Specificities of Four Exo-Type Cellulases Produced by Aspergillus niger, Trichoderma reesei, and Irpex lacteus on (1->3),(1->4)- -D-Glucans and Xyloglucan Amano, Y.; Shiroishi, M.; Nisizawa, K. Journal of Biochemistry, Vol. 120, Issue 6 https://doi.org/10.1093/oxfordjournals.jbchem.a021531	journal	December 1996
Gene sequence and properties of Cell, a family E endoglucanase from Clostridium thermocellum Hazlewood,, G. P.; Davidson, K.; Laurie, J. I. Journal of General Microbiology, Vol. 139, Issue 2 https://doi.org/10.1099/00221287-139-2-307	journal	February 1993
Cell-free protein synthesis and substrate specificity of full-length endoglucanase CelJ (Cel9D-Cel44A), the largest multi-enzyme subunit of theClostridium thermocellumcellulosome Hirano, Nobutaka; Hasegawa, Hiroki; Nihei, Satoshi FEMS Microbiology Letters, Vol. 344, Issue 1 https://doi.org/10.1111/1574-6968.12149	journal	April 2013
Structure of the beta-glucosidase gene bglA of Clostridium thermocellum. Sequence analysis reveals a superfamily of cellulases and beta-glycosidases including human lactase/phlorizin hydrolase Grabnitz, Folke; Seiss, Monika; Rucknagel, Karl P. European Journal of Biochemistry, Vol. 200, Issue 2 https://doi.org/10.1111/j.1432-1033.1991.tb16186.x	journal	September 1991
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Stoichiometric Assembly of the Cellulosome Generates Maximum Synergy for the Degradation of Crystalline Cellulose, as Revealed by In Vitro Reconstitution of the Clostridium thermocellum Cellulosome Hirano, Katsuaki; Nihei, Satoshi; Hasegawa, Hiroki Applied and Environmental Microbiology, Vol. 81, Issue 14 https://doi.org/10.1128/AEM.00772-15	journal	July 2015
Global Gene Expression Patterns in Clostridium thermocellum as Determined by Microarray Analysis of Chemostat Cultures on Cellulose or Cellobiose Riederer, Allison; Takasuka, Taichi E.; Makino, Shin-ichi Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/AEM.02008-10	journal	December 2010
Complete Genome Sequence of the Cellulolytic Thermophile Clostridium thermocellum DSM1313 Feinberg, L.; Foden, J.; Barrett, T. Journal of Bacteriology, Vol. 193, Issue 11, p. 2906-2907 https://doi.org/10.1128/JB.00322-11	journal	April 2011
Global View of the Clostridium thermocellum Cellulosome Revealed by Quantitative Proteomic Analysis Gold, N. D.; Martin, V. J. J. Journal of Bacteriology, Vol. 189, Issue 19 https://doi.org/10.1128/JB.00882-07	journal	July 2007
Cloning and Sequence Analysis of a New Cellulase Gene Encoding CelK, a Major Cellulosome Component of Clostridium thermocellum: Evidence for Gene Duplication and Recombination Kataeva, Irina; Li, Xin-Liang; Chen, Huizhong Journal of Bacteriology, Vol. 181, Issue 17 https://doi.org/10.1128/JB.181.17.5288-5295.1999	journal	September 1999
Cellulosomes: Highly Efficient Nanomachines Designed to Deconstruct Plant Cell Wall Complex Carbohydrates Fontes, Carlos M. G. A.; Gilbert, Harry J. Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev-biochem-091208-085603	journal	June 2010
Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation Raman, Babu; McKeown, Catherine K; Rodriguez, Miguel BMC Microbiology, Vol. 11, Issue 1, Article No. 134 https://doi.org/10.1186/1471-2180-11-134	journal	January 2011
Genome-scale metabolic analysis of Clostridium thermocellum for bioethanol production Roberts, Seth B.; Gowen, Christopher M.; Brooks, J. Paul BMC Systems Biology, Vol. 4, Issue 1, Article No. 31 https://doi.org/10.1186/1752-0509-4-31	journal	January 2010
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
Automated Filter Paper Assay for Determination of Cellulase Activity Decker, Stephen R.; Adney, William S.; Jennings, Edward Applied Biochemistry and Biotechnology, Vol. 107, Issue 1-3 https://doi.org/10.1385/ABAB:107:1-3:689	journal	January 2003
Cellulase activities in biomass conversion: measurement methods and comparison Dashtban, Mehdi; Maki, Miranda; Leung, Kam Tin Critical Reviews in Biotechnology, Vol. 30, Issue 4 https://doi.org/10.3109/07388551.2010.490938	journal	June 2010

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Determination of glycoside hydrolase specificities during hydrolysis of plant cell walls using glycome profiling Walker, Johnnie A.; Pattathil, Sivakumar; Bergeman, Lai F. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0703-6	journal	February 2017

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