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Discovery and characterization of family 39 glycoside hydrolases from rumen anaerobic fungi with polyspecific activity on rare arabinosyl substrates

Title:

Discovery and characterization of family 39 glycoside hydrolases from rumen anaerobic fungi with polyspecific activity on rare arabinosyl substrates

Jones, Darryl R., Uddin, Muhammed Salah, Gruninger, Robert J., Pham, Thi Thanh My, Thomas, Dallas, Boraston, Alisdair B., Briggs, Jonathan, Pluvinage, Benjamin, McAllister, Tim A., Forster, Robert J., Tsang, Adrian, Selinger, L. Brent and Abbott, D. Wade (2017) Discovery and characterization of family 39 glycoside hydrolases from rumen anaerobic fungi with polyspecific activity on rare arabinosyl substrates. Journal of Biological Chemistry, 292 (30). pp. 12606-12620. ISSN 0021-9258

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Official URL: http://dx.doi.org/10.1074/jbc.M117.789008

Abstract

Enzyme activities that improve digestion of recalcitrant plant cell wall polysaccharides may offer solutions for sustainable industries. To this end, anaerobic fungi in the rumen have been identified as a promising source of novel carbohydrate active enzymes (CAZymes) that modify plant cell wall polysaccharides and other complex glycans. Many CAZymes share insufficient sequence identity to characterized proteins from other microbial ecosystems to infer their function; thus presenting challenges to their identification. In this study, four rumen fungal genes (nf2152, nf2215, nf2523, and pr2455) were identified that encode family 39 glycoside hydrolases (GH39s), and have conserved structural features with GH51s. Two recombinant proteins, NF2152 and NF2523, were characterized using a variety of biochemical and structural techniques, and were determined to have distinct catalytic activities. NF2152 releases a single product, β1,2-arabinobiose (Ara2) from sugar beet arabinan (SBA), and β1,2-Ara2 and α-1,2-galactoarabinose (Gal-Ara) from rye arabinoxylan (RAX). NF2523 exclusively releases α-1,2-Gal-Ara from RAX, which represents the first description of a galacto-(α-1,2)-arabinosidase. Both β-1,2-Ara2 and α-1,2-Gal-Ara are disaccharides not previously described within SBA and RAX. In this regard, the enzymes studied here may represent valuable new biocatalytic tools for investigating the structures of rare arabinosyl-containing glycans, and potentially for facilitating their modification in industrial applications.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Refereed:Yes
Authors:Jones, Darryl R. and Uddin, Muhammed Salah and Gruninger, Robert J. and Pham, Thi Thanh My and Thomas, Dallas and Boraston, Alisdair B. and Briggs, Jonathan and Pluvinage, Benjamin and McAllister, Tim A. and Forster, Robert J. and Tsang, Adrian and Selinger, L. Brent and Abbott, D. Wade
Journal or Publication:Journal of Biological Chemistry
Date:6 June 2017
Funders:
  • Agriculture and Agri-Food Canada (AAFC) through Agriculture Innovation Program Grant AIP-P022 and Elanco Animal Health
  • Natural Sciences and Engineering Research Council of Canada Discovery Grant FRN 04355 (to A. B. B.)
Digital Object Identifier (DOI):10.1074/jbc.M117.789008
Keywords:carbohydrate, enzyme, fungi, galactose, glycoside hydrolase, arabinose, rumen
ID Code:983684
Deposited By: Monique Lane
Deposited On:05 Apr 2018 19:41
Last Modified:06 Jun 2018 00:00

References:

Morgavi, D. P., Kelly, W. J., Janssen, P. H., and Attwood, G. T. (2013) Rumen microbial (meta)genomics and its application to ruminant production. Animal 7, 184–201

Ribeiro, G. O., Gruninger, R., Badhan, A., and McAllister, T. A. (2016) Mining the rumen for fibrolytic feed enzymes. Animal Front. 6, 20–26

Hess, M., Sczyrba, A., Egan, R., Kim, T. W., Chokhawala, H., Schroth, G., Luo, S., Clark, D. S., Chen, F., Zhang, T., ackie, R. I., Pennacchio, L. A., Tringe, S. G., Visel, A., Woyke, T., Wang, Z., and Rubin, E. M. (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331, 463–467

Qi, M., Wang, P., O'Toole, N., Barboza, P. S., Ungerfeld, E., Leigh, M. B., Selinger, L. B., Butler, G., Tsang, A., McAllister, T. A., and Forster, R. J. (2011) Snapshot of the eukaryotic gene expression in muskoxen rumen: a metatranscriptomic approach. PloS One 6, e20521

Dai, X., Tian, Y., Li, J., Luo, Y., Liu, D., Zheng, H., Wang, J., Dong, Z., Hu, S., and Huang, L. (2015) Metatranscriptomic analyses of plant cell wall polysaccharide degradation by microorganisms in the cow rumen. Appl. Environ. Microbiol. 81, 1375–1386

Houston, K., Tucker, M. R., Chowdhury, J., Shirley, N., and Little, A. (2016) The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front. Plant Sci. 7, 984

Mohnen, D., Bar-Peled, M., and Somerville, C. (2008) Cell wall polysaccharide synthesis. Biomass Recalcitrance: Deconstructing Plant Cell Wall Bioenergy, pp. 94–187,Blackwell Publishing, John Wiley and Sons, Hoboken, NJ

Bengtsson, S., Åman, P., and Andersson, R. (1992) Structural studies on water-soluble arabinoxylans in rye grain using enzymatic hydrolysis. Carbohydr. Polymers 17, 277–284

Jarvis, M., Briggs, S., and Knox, J. (2003) Intercellular adhesion and cell separation in plants. Plant Cell Environ. 26, 977–989

Atmodjo, M. A., Hao, Z., and Mohnen, D. (2013) Evolving views of pectin biosynthesis. Annu. Rev. Plant Biol. 64, 747–779

Ndeh, D., Rogowski, A., Cartmell, A., Luis, A. S., Baslé, A., Gray, J., Venditto, I., Briggs, J., Zhang, X., Labourel, A., Terrapon, N., Buffetto, F., Nepogodiev, S., Xiao, Y., Field, R. A., et al . (2017) Complex pectin metabolism by gut bacteria reveals novel catalytic functions.Nature 544, 65–70

Jones, L., Milne, J. L., Ashford, D., and McQueen-Mason, S. J. (2003) Cell wall arabinan is essential for guard cell function. Proc. Natl. Acad. Sci. U.S.A. 100, 11783–11788

Showalter, A. M. (2001) Arabinogalactan-proteins: structure, expression and function. Cell. Mol. Life Sci. 58, 1399–1417

Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., and Henrissat, B. (2014)The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42,D490–D495

Mewis, K., Lenfant, N., Lombard, V., and Henrissat, B. (2016) Dividing the large glycoside hydrolase family 43 into subfamilies: a motivation for detailed enzyme characterization. Appl. Environ. Microbiol. 82, 1686–1692

Aspeborg, H., Coutinho, P. M., Wang, Y., Brumer, H., 3rd., and Henrissat, B. (2012)Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol. Biol. 12, 186

Davies, G., and Henrissat, B. (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3, 853–859

Boraston, A. B., Bolam, D. N., Gilbert, H. J., and Davies, G. J. (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382, 769–781

Fujimoto, Z. (2013) Structure and function of carbohydrate-binding module families 13 and 42 of glycoside hydrolases, comprising a beta-trefoil fold. Biosci. Biotechnol. Biochem. 77, 1363–1371

Solomon, K. V., Haitjema, C. H., Henske, J. K., Gilmore, S. P., Borges-Rivera, D., Lipzen, A., Brewer, H. M.,
Purvine, S. O., Wright, A. T., Theodorou, M. K., Grigoriev, I. V., Regev, A., Thompson, D. A., and O'Malley, M. A. (2016) Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes. Science 351, 1192–1195

Badhan, A., Wang, Y., Gruninger, R., Patton, D., Powlowski, J., Tsang, A., and McAllister, T. (2014) Formulation of enzyme blends to maximize the hydrolysis of alkaline peroxide pretreated alfalfa hay and barley straw by rumen enzymes and commercial cellulases.BMC Biotechnol. 14, 31

Gruninger, R. J., Puniya, A. K., Callaghan, T. M., Edwards, J. E., Youssef, N., Dagar, S. S., Fliegerova, K., Griffith, G. W., Forster, R., Tsang, A., McAllister, T., and Elshahed, M. S. (2014)Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential. FEMS Microbiol. Ecol.90, 1–17

Couger, M. B., Youssef, N. H., Struchtemeyer, C. G., Liggenstoffer, A. S., and Elshahed, M. S. (2015) Transcriptomic analysis of lignocellulosic biomass degradation by the anaerobic fungal isolate Orpinomyces sp. strain C1A. Biotechnol. Biofuels 8, 208

Morrison, J. M., Elshahed, M. S., and Youssef, N. (2016) A multifunctional GH39 glycoside hydrolase from the anaerobic gut fungus Orpinomyces sp. strain C1A. Peer J.4, e2289

Fujita, K., Takashi, Y., Obuchi, E., Kitahara, K., and Suganuma, T. (2014)Characterization of a novel β-L-arabinofuranosidase in Bifidobacterium longumfuntional elucidation of a DUF1680 protein family member. J. Biol. Chem. 289, 5240–5249

Yapo, B. M. (2011) Rhamnogalacturonan-I: a structurally puzzling and functionally versatile polysaccharide from plant cell walls and mucilages. Polymer Rev. 51, 391–413

Fujita, K., Sakamoto, S., Ono, Y., Wakao, M., Suda, Y., Kitahara, K., and Suganuma, T. (2011) Molecular cloning and characterization of a β-L-arabinobiosidase in Bifidobacterium longum that belongs to a novel glycoside hydrolase family. J. Biol. Chem. 286, 5143–5150

Bock, K., Pedersen, C., and Pedersen, H. (1984) Carbon-13 nuclear magnetic resonance data for oligosaccharides. Adv. Carbohydr. Chem. Biochem. 42, 193–225

Duus, J., Gotfredsen, C. H., and Bock, K. (2000) Carbohydrate structural determination by NMR spectroscopy: modern methods and limitations. Chem. Rev.100, 4589–4614

Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D.Nucleic Acids Res. 38, W545–W549

Santos, C. R., Polo, C. C., Corrêa, J. M., Simão Rde, C., Seixas, F. A., and Murakami, M. T. (2012) The accessory domain changes the accessibility and molecular topography of the catalytic interface in monomeric GH39 beta-xylosidases. Acta Crystallogr. D Biol. Crystallogr. 68, 1339–1345

Paës, G., Skov, L. K., O'Donohue, M. J., Rémond, C., Kastrup, J. S., Gajhede, M., and Mirza, O. (2008) The structure of the complex between a branched pentasaccharide and Thermobacillus xylanilyticus GH-51 arabinofuranosidase reveals xylan-binding determinants and induced fit. Biochemistry 47, 7441–7451

Sainz-Polo, M. A., Valenzuela, S. V., González, B., Pastor, F. I., and Sanz-Aparicio, J. (2014)Structural analysis of glucuronoxylan-specific Xyn30D and its attached CBM35 domain gives insights into the role of modularity in specificity. J. Biol. Chem. 289, 31088–31101

Im, D. H., Kimura, K., Hayasaka, F., Tanaka, T., Noguchi, M., Kobayashi, A., Shoda, S., Miyazaki, K., Wakagi, T., and
Fushinobu, S. (2012) Crystal structures of glycoside hydrolase family 51 α-L-arabinofuranosidase from Thermotoga maritima. Biosci. Biotechnol. Biochem. 76, 423–428

Read, R. J. (1986) Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallog. Sect. A 42, 140–149

Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M.,
Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Systems Biol. 7, 539

Goldenberg, O., Erez, E., Nimrod, G., and Ben-Tal, N. (2009) The ConSurf-DB: pre-calculated evolutionary conservation profiles of protein structures. Nucleic Acids Res.37, D323–D327

Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233–D238

Shi, H., Ding, H., Huang, Y., Wang, L., Zhang, Y., Li, X., and Wang, F. (2014) Expression and characterization of a GH43 endo-arabinanase from Thermotoga thermarum. BMC Biotechnol. 14, 35

Sakamoto, T., and Thibault, J.-F. (2001) Exo-arabinanase of Penicillium chrysogenum able to release arabinobiose from α-1,5-L-arabinan. Appl. Environ. Microbiol. 67, 3319–3321

Santos, C. R., Polo, C. C., Costa, M. C., Nascimento, A. F., Meza, A. N., Cota, J., Hoffmam, Z. B., Honorato, R. V.,
Oliveira, P. S., Goldman, G. H., et al . (2014) Mechanistic strategies for catalysis adopted by evolutionary distinct family 43 arabinanases. J. Biol. Chem. 289, 7362–7373

Vinkx, C., and Delcour, J. (1996) Rye (Secale cereale L.) Arabinoxylans: a critical review. J. Cereal Sci. 24, 1–14

Vinkx, C., Reynaert, H., Grobet, P., and Delcour, J. (1993) Physicochemical and functional properties of rye nonstarch polysaccharides: V. variability in the structure of water-soluble arabinoxylans. Cereal Chem. 70, 311–311

Collins, T., Gerday, C., and Feller, G. (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol. Rev. 29, 3–23

Tefsen, B., Ram, A. F., van Die, I., and Routier, F. H. (2012) Galactofuranose in eukaryotes: aspects of biosynthesis and functional impact. Glycobiology 22, 456–469

Tóth-Petróczy, A., and Tawfik, D. S. (2014) The robustness and innovability of protein folds. Curr. Opin. Struct. Biol. 26, 131–138

Tan, L., Eberhard, S., Pattathil, S., Warder, C., Glushka, J., Yuan, C., Hao, Z., Zhu, X., Avci, U., Miller, J. S., ldwin, D., Pham, C., Orlando, R., Darvill, A., Hahn, M. G., Kieliszewski, M. J., and Mohnen, D. (2013) An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25, 270–287

Yin, Y., Mao, X., Yang, J., Chen, X., Mao, F., and Xu, Y. (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40, W445–W451

Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797

Price, M. N., Dehal, P. S., and Arkin, A. P. (2010) FastTree 2: approximately maximum-likelihood trees for large alignments. PloS One 5, e9490

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164–1165

Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S. e., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy server.Methods Mol. Biol. 112, 531–552

Blakeney, A. B., Harris, P. J., Henry, R. J., and Stone, B. A. (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr. Res. 113, 291–299

Gao, N. (2005) Fluorophore-assisted carbohydrate electrophoresis: a sensitive and accurate method for the direct analysis of dolichol pyrophosphate-linked oligosaccharides in cell cultures and tissues. Methods 35, 323–327

Joseleau, J.-P., Chambat, G., Vignon, M., and Barnoud, F. (1977) Chemical and 13C NMR studies of two arabinans from the inner bark of young stems of Rosa Glauca.Carbohydr. Res. 58, 165–175

Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326

Sheldrick, G. M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479–485

Schneider, T. R., and Sheldrick, G. M. (2002) Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772–1779

McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674

Cowtan, K. (2010) Recent developments in classical density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 470–478

Cowtan, K. (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002–1011

Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760–763
Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7.Nature Protoc. 3, 1171–1179

Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132

Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G..,
Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al . (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66,213–221

Brünger, A. T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472–475

Chen, V. B., Arendall, W. B., 3rd., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W.,
Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66,12–21

McLean, R., Hobbs, J. K., Suits, M. D., Tuomivaara, S. T., Jones, D. R., Boraston, A. B., and Abbott, D. W. (2015) Functional analyses of resurrected and contemporary enzymes illuminate an evolutionary path for the emergence of exolysis in polysaccharide lyase family 2. J. Biol. Chem. 290, 21231–21243

Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240–255

Rambaut, A. (2014) FigTree – Tree Figure Drawing Tool, Version 1.4.2, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom

Woods Group (2017) Carbohydrate Builder – GLYCAM Web, Complex Carbohydrate Research Center, University of Georgia, Athens, GA
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