Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry

Heins RA, Cheng X, Nath S, Deng K, Bowen BP, Chivian DC, Datta S, Friedland GD, D'Haeseleer P, Wu D, Tran-Gyamfi M, et al. (2014)
ACS chemical biology 9(9): 2082-2091.

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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
Harnessing the biotechnological potential of the large number of proteins available in sequence databases requires scalable methods for functional characterization. Here we propose a workflow to address this challenge by combining phylogenomic guided DNA synthesis with high-throughput mass spectrometry and apply it to the systematic characterization of GH1 β-glucosidases, a family of enzymes necessary for biomass hydrolysis, an important step in the conversion of lignocellulosic feedstocks to fuels and chemicals. We synthesized and expressed 175 GH1s, selected from over 2000 candidate sequences to cover maximum sequence diversity. These enzymes were functionally characterized over a range of temperatures and pHs using nanostructure-initiator mass spectrometry (NIMS), generating over 10,000 data points. When combined with HPLC-based sugar profiling, we observed GH1 enzymes active over a broad temperature range and toward many different β-linked disaccharides. For some GH1s we also observed activity toward laminarin, a more complex oligosaccharide present as a major component of macroalgae. An area of particular interest was the identification of GH1 enzymes compatible with the ionic liquid 1-ethyl-3-methylimidazolium acetate ([C2mim][OAc]), a next-generation biomass pretreatment technology. We thus searched for GH1 enzymes active at 70 °C and 20% (v/v) [C2mim][OAc] over the course of a 24-h saccharification reaction. Using our unbiased approach, we identified multiple enzymes of different phylogentic origin with such activities. Our approach of characterizing sequence diversity through targeted gene synthesis coupled to high-throughput screening technologies is a broadly applicable paradigm for a wide range of biological problems.
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ACS chemical biology
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9
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9
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2082-2091
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Heins RA, Cheng X, Nath S, et al. Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry. ACS chemical biology. 2014;9(9):2082-2091.
Heins, R. A., Cheng, X., Nath, S., Deng, K., Bowen, B. P., Chivian, D. C., Datta, S., et al. (2014). Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry. ACS chemical biology, 9(9), 2082-2091. doi:10.1021/cb500244v
Heins, R. A., Cheng, X., Nath, S., Deng, K., Bowen, B. P., Chivian, D. C., Datta, S., Friedland, G. D., D'Haeseleer, P., Wu, D., et al. (2014). Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry. ACS chemical biology 9, 2082-2091.
Heins, R.A., et al., 2014. Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry. ACS chemical biology, 9(9), p 2082-2091.
R.A. Heins, et al., “Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry”, ACS chemical biology, vol. 9, 2014, pp. 2082-2091.
Heins, R.A., Cheng, X., Nath, S., Deng, K., Bowen, B.P., Chivian, D.C., Datta, S., Friedland, G.D., D'Haeseleer, P., Wu, D., Tran-Gyamfi, M., Scullin, C.S., Singh, S., Shi, W., Hamilton, M.G., Bendall, M.L., Sczyrba, A., Thompson, J., Feldman, T., Guenther, J.M., Gladden, J.M., Cheng, J.-F., Adams, P.D., Rubin, E.M., Simmons, B.A., Sale, K.L., Northen, T.R., Deutsch, S.: Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry. ACS chemical biology. 9, 2082-2091 (2014).
Heins, Richard A, Cheng, Xiaoliang, Nath, Sangeeta, Deng, Kai, Bowen, Benjamin P, Chivian, Dylan C, Datta, Supratim, Friedland, Gregory D, D'Haeseleer, Patrik, Wu, Dongying, Tran-Gyamfi, Mary, Scullin, Chessa S, Singh, Seema, Shi, Weibing, Hamilton, Matthew G, Bendall, Matthew L, Sczyrba, Alexander, Thompson, John, Feldman, Taya, Guenther, Joel M, Gladden, John M, Cheng, Jan-Fang, Adams, Paul D, Rubin, Edward M, Simmons, Blake A, Sale, Kenneth L, Northen, Trent R, and Deutsch, Samuel. “Phylogenomically Guided Identification of Industrially Relevant GH1 β-Glucosidases through DNA Synthesis and Nanostructure-Initiator Mass Spectrometry”. ACS chemical biology 9.9 (2014): 2082-2091.

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Dossani ZY, Reider Apel A, Szmidt-Middleton H, Hillson NJ, Deutsch S, Keasling JD, Mukhopadhyay A., Yeast 35(3), 2018
PMID: 29084380
Metagenomic Analysis of Bacteria, Fungi, Bacteriophages, and Helminths in the Gut of Giant Pandas.
Yang S, Gao X, Meng J, Zhang A, Zhou Y, Long M, Li B, Deng W, Jin L, Zhao S, Wu D, He Y, Li C, Liu S, Huang Y, Zhang H, Zou L., Front Microbiol 9(), 2018
PMID: 30108570
Exploiting non-conserved residues to improve activity and stability of Halothermothrix orenii β-glucosidase.
Sinha SK, Goswami S, Das S, Datta S., Appl Microbiol Biotechnol 101(4), 2017
PMID: 27761638
On-chip integration of droplet microfluidics and nanostructure-initiator mass spectrometry for enzyme screening.
Heinemann J, Deng K, Shih SC, Gao J, Adams PD, Singh AK, Northen TR., Lab Chip 17(2), 2017
PMID: 27957569
Investigation of Proposed Ladderane Biosynthetic Genes from Anammox Bacteria by Heterologous Expression in E. coli.
Javidpour P, Deutsch S, Mutalik VK, Hillson NJ, Petzold CJ, Keasling JD, Beller HR., PLoS One 11(3), 2016
PMID: 26975050
Biofuel metabolic engineering with biosensors.
Morgan SA, Nadler DC, Yokoo R, Savage DF., Curr Opin Chem Biol 35(), 2016
PMID: 27768949
Exploiting members of the BAHD acyltransferase family to synthesize multiple hydroxycinnamate and benzoate conjugates in yeast.
Eudes A, Mouille M, Robinson DS, Benites VT, Wang G, Roux L, Tsai YL, Baidoo EE, Chiu TY, Heazlewood JL, Scheller HV, Mukhopadhyay A, Keasling JD, Deutsch S, Loqué D., Microb Cell Fact 15(1), 2016
PMID: 27871334
High throughput screening of enzyme activity with mass spectrometry imaging.
de Rond T, Danielewicz M, Northen T., Curr Opin Biotechnol 31(), 2015
PMID: 25129648
Biocatalysts for biomass deconstruction from environmental genomics.
Armstrong Z, Mewis K, Strachan C, Hallam SJ., Curr Opin Chem Biol 29(), 2015
PMID: 26231123
Development of a High Throughput Platform for Screening Glycoside Hydrolases Based on Oxime-NIMS.
Deng K, Guenther JM, Gao J, Bowen BP, Tran H, Reyes-Ortiz V, Cheng X, Sathitsuksanoh N, Heins R, Takasuka TE, Bergeman LF, Geertz-Hansen H, Deutsch S, Loqué D, Sale KL, Simmons BA, Adams PD, Singh AK, Fox BG, Northen TR., Front Bioeng Biotechnol 3(), 2015
PMID: 26528471
Use of Nanostructure-Initiator Mass Spectrometry to Deduce Selectivity of Reaction in Glycoside Hydrolases.
Deng K, Takasuka TE, Bianchetti CM, Bergeman LF, Adams PD, Northen TR, Fox BG., Front Bioeng Biotechnol 3(), 2015
PMID: 26579511
Integrative genomic mining for enzyme function to enable engineering of a non-natural biosynthetic pathway.
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PMID: 26598135

33 References

Daten bereitgestellt von Europe PubMed Central.

Metagenomics: DNA sequencing of environmental samples.
Tringe SG, Rubin EM., Nat. Rev. Genet. 6(11), 2005
PMID: 16304596
Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina.
Kubicek CP, Mikus M, Schuster A, Schmoll M, Seiboth B., Biotechnol Biofuels 2(), 2009
PMID: 19723296
Inhibition of the Trichoderma reesei cellulases by cellobiose is strongly dependent on the nature of the substrate.
Gruno M, Valjamae P, Pettersson G, Johansson G., Biotechnol. Bioeng. 86(5), 2004
PMID: 15129433
β-Glucosidases.
Ketudat Cairns JR, Esen A., Cell. Mol. Life Sci. 67(20), 2010
PMID: 20490603
Crystal structure of beta-glucosidase A from Bacillus polymyxa: insights into the catalytic activity in family 1 glycosyl hydrolases.
Sanz-Aparicio J, Hermoso JA, Martinez-Ripoll M, Lequerica JL, Polaina J., J. Mol. Biol. 275(3), 1998
PMID: 9466926
The crystal structure of beta-glucosidase from Bacillus circulans sp. alkalophilus: ability to form long polymeric assemblies.
Hakulinen N, Paavilainen S, Korpela T, Rouvinen J., J. Struct. Biol. 129(1), 2000
PMID: 10675298
Structural and functional analysis of three β-glucosidases from bacterium Clostridium cellulovorans, fungus Trichoderma reesei and termite Neotermes koshunensis.
Jeng WY, Wang NC, Lin MH, Lin CT, Liaw YC, Chang WJ, Liu CI, Liang PH, Wang AH., J. Struct. Biol. 173(1), 2010
PMID: 20682343
Mechanism of Agrobacterium beta-glucosidase: kinetic studies.
Kempton JB, Withers SG., Biochemistry 31(41), 1992
PMID: 1390780
Mechanistic insights into glycosidase chemistry.
Vocadlo DJ, Davies GJ., Curr Opin Chem Biol 12(5), 2008
PMID: 18558099
Biomass pretreatment: fundamentals toward application.
Agbor VB, Cicek N, Sparling R, Berlin A, Levin DB., Biotechnol. Adv. 29(6), 2011
PMID: 21624451
Biomass deconstruction to sugars.
Blanch HW, Simmons BA, Klein-Marcuschamer D., Biotechnol J 6(9), 2011
PMID: 21834132
Acoustic deposition with NIMS as a high-throughput enzyme activity assay.
Greving M, Cheng X, Reindl W, Bowen B, Deng K, Louie K, Nyman M, Cohen J, Singh A, Simmons B, Adams P, Siuzdak G, Northen T., Anal Bioanal Chem 403(3), 2012
PMID: 22407334
A nanostructure-initiator mass spectrometry-based enzyme activity assay.
Northen TR, Lee JC, Hoang L, Raymond J, Hwang DR, Yannone SM, Wong CH, Siuzdak G., Proc. Natl. Acad. Sci. U.S.A. 105(10), 2008
PMID: 18319341
Metagenomic discovery of biomass-degrading genes and genomes from cow rumen.
Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM., Science 331(6016), 2011
PMID: 21273488
A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea.
Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D'haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng JF, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk HP, Eisen JA., Nature 462(7276), 2009
PMID: 20033048
Encoding substrates with mass tags to resolve stereospecific reactions using Nimzyme.
Deng K, George KW, Reindl W, Keasling JD, Adams PD, Lee TS, Singh AK, Northen TR., Rapid Commun. Mass Spectrom. 26(6), 2012
PMID: 22328213
An engineered microbial platform for direct biofuel production from brown macroalgae.
Wargacki AJ, Leonard E, Win MN, Regitsky DD, Santos CN, Kim PB, Cooper SR, Raisner RM, Herman A, Sivitz AB, Lakshmanaswamy A, Kashiyama Y, Baker D, Yoshikuni Y., Science 335(6066), 2012
PMID: 22267807
Computational analysis of glycoside hydrolase family 1 specificities.
Hill AD, Reilly PJ., Biopolymers 89(11), 2008
PMID: 18615662
GH1-family 6-P-β-glucosidases from human microbiome lactic acid bacteria.
Michalska K, Tan K, Li H, Hatzos-Skintges C, Bearden J, Babnigg G, Joachimiak A., Acta Crystallogr. D Biol. Crystallogr. 69(Pt 3), 2013
PMID: 23519420
Structural insights into the substrate specificity of a 6-phospho-β-glucosidase BglA-2 from Streptococcus pneumoniae TIGR4.
Yu WL, Jiang YL, Pikis A, Cheng W, Bai XH, Ren YM, Thompson J, Zhou CZ, Chen Y., J. Biol. Chem. 288(21), 2013
PMID: 23580646
Structure and activity of the Streptococcus pyogenes family GH1 6-phospho-β-glucosidase SPy1599.
Stepper J, Dabin J, Eklof JM, Thongpoo P, Kongsaeree P, Taylor EJ, Turkenburg JP, Brumer H, Davies GJ., Acta Crystallogr. D Biol. Crystallogr. 69(Pt 1), 2012
PMID: 23275159
A thermophilic ionic liquid-tolerant cellulase cocktail for the production of cellulosic biofuels.
Park JI, Steen EJ, Burd H, Evans SS, Redding-Johnson AM, Batth T, Benke PI, D'haeseleer P, Sun N, Sale KL, Keasling JD, Lee TS, Petzold CJ, Mukhopadhyay A, Singer SW, Simmons BA, Gladden JM., PLoS ONE 7(5), 2012
PMID: 22649505
Search and clustering orders of magnitude faster than BLAST.
Edgar RC., Bioinformatics 26(19), 2010
PMID: 20709691
FastTree: computing large minimum evolution trees with profiles instead of a distance matrix.
Price MN, Dehal PS, Arkin AP., Mol. Biol. Evol. 26(7), 2009
PMID: 19377059
Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy.
Letunic I, Bork P., Nucleic Acids Res. 39(Web Server issue), 2011
PMID: 21470960
Parallel on-chip gene synthesis and application to optimization of protein expression.
Quan J, Saaem I, Tang N, Ma S, Negre N, Gong H, White KP, Tian J., Nat. Biotechnol. 29(5), 2011
PMID: 21516083
GeneDesign 3.0 is an updated synthetic biology toolkit.
Richardson SM, Nunley PW, Yarrington RM, Boeke JD, Bader JS., Nucleic Acids Res. 38(8), 2010
PMID: 20211837
Colloid-based multiplexed screening for plant biomass-degradingglycoside hydrolase activities in microbial communities
AUTHOR UNKNOWN, 2011
One-pot ionic liquid pretreatmentand saccharification of switchgrass
AUTHOR UNKNOWN, 2013
Biochemical characterization and crystal structure of endoglucanase Cel5A from the hyperthermophilic Thermotoga maritima.
Pereira JH, Chen Z, McAndrew RP, Sapra R, Chhabra SR, Sale KL, Simmons BA, Adams PD., J. Struct. Biol. 172(3), 2010
PMID: 20599513

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