2whk › Citations

Understanding how diverse beta-mannanases recognize heterogeneous substrates.

Tailford LE, Ducros VM, Flint JE, Roberts SM, Morland C, Zechel DL, Smith N, Bjørnvad ME, Borchert TV, Wilson KS, Davies GJ, Gilbert HJ
Biochemistry 48 7009-18 (2009)
Related entries: 2whj, 2whl, 2whm

Cited: 56 times
EuropePMC logo PMID: 19441796

Abstract

The mechanism by which polysaccharide-hydrolyzing enzymes manifest specificity toward heterogeneous substrates, in which the sequence of sugars is variable, is unclear. An excellent example of such heterogeneity is provided by the plant structural polysaccharide glucomannan, which comprises a backbone of beta-1,4-linked glucose and mannose units. beta-Mannanases, located in glycoside hydrolase (GH) families 5 and 26, hydrolyze glucomannan by cleaving the glycosidic bond of mannosides at the -1 subsite. The mechanism by which these enzymes select for glucose or mannose at distal subsites, which is critical to defining their substrate specificity on heterogeneous polymers, is currently unclear. Here we report the biochemical properties and crystal structures of both a GH5 mannanase and a GH26 mannanase and describe the contributions to substrate specificity in these enzymes. The GH5 enzyme, BaMan5A, derived from Bacillus agaradhaerens, can accommodate glucose or mannose at both its -2 and +1 subsites, while the GH26 Bacillus subtilis mannanase, BsMan26A, displays tight specificity for mannose at its negative binding sites. The crystal structure of BaMan5A reveals that a polar residue at the -2 subsite can make productive contact with the substrate 2-OH group in either its axial (as in mannose) or its equatorial (as in glucose) configuration, while other distal subsites do not exploit the 2-OH group as a specificity determinant. Thus, BaMan5A is able to hydrolyze glucomannan in which the sequence of glucose and mannose is highly variable. The crystal structure of BsMan26A in light of previous studies on the Cellvibrio japonicus GH26 mannanases CjMan26A and CjMan26C reveals that the tighter mannose recognition at the -2 subsite is mediated by polar interactions with the axial 2-OH group of a (4)C(1) ground state mannoside. Mutagenesis studies showed that variants of CjMan26A, from which these polar residues had been removed, do not distinguish between Man and Glc at the -2 subsite, while one of these residues, Arg 361, confers the elevated activity displayed by the enzyme against mannooligosaccharides. The biological rationale for the variable recognition of Man- and Glc-configured sugars by beta-mannanases is discussed.

Articles - 2whk mentioned but not cited (3)

  1. Structural and biochemical analyses of glycoside hydrolase families 5 and 26 β-(1,4)-mannanases from Podospora anserina reveal differences upon manno-oligosaccharide catalysis. Couturier M, Roussel A, Rosengren A, Leone P, Stålbrand H, Berrin JG. J Biol Chem 288 14624-14635 (2013)
  2. Structural and biochemical analyses of glycoside hydrolase family 26 β-mannanase from a symbiotic protist of the termite Reticulitermes speratus. Tsukagoshi H, Nakamura A, Ishida T, Touhara KK, Otagiri M, Moriya S, Samejima M, Igarashi K, Fushinobu S, Kitamoto K, Arioka M. J Biol Chem 289 10843-10852 (2014)
  3. Spatially remote motifs cooperatively affect substrate preference of a ruminal GH26-type endo-β-1,4-mannanase. Mandelli F, de Morais MAB, de Lima EA, Oliveira L, Persinoti GF, Murakami MT. J Biol Chem 295 5012-5021 (2020)


Reviews citing this publication (9)

  1. The biochemistry and structural biology of plant cell wall deconstruction. Gilbert HJ. Plant Physiol 153 444-455 (2010)
  2. Mannanases: microbial sources, production, properties and potential biotechnological applications. Chauhan PS, Puri N, Sharma P, Gupta N. Appl Microbiol Biotechnol 93 1817-1830 (2012)
  3. A review of the enzymatic hydrolysis of mannans and synergistic interactions between β-mannanase, β-mannosidase and α-galactosidase. Malgas S, van Dyk JS, Pletschke BI. World J Microbiol Biotechnol 31 1167-1175 (2015)
  4. Production, properties, and applications of endo-β-mannanases. Srivastava PK, Kapoor M. Biotechnol Adv 35 1-19 (2017)
  5. Applications of Microbial β-Mannanases. Dawood A, Ma K. Front Bioeng Biotechnol 8 598630 (2020)
  6. Mannoside recognition and degradation by bacteria. Ladevèze S, Laville E, Despres J, Mosoni P, Potocki-Véronèse G. Biol Rev Camb Philos Soc 92 1969-1990 (2017)
  7. Enzymatic Conversion of Mannan-Rich Plant Waste Biomass into Prebiotic Mannooligosaccharides. Hlalukana N, Magengelele M, Malgas S, Pletschke BI. Foods 10 2010 (2021)
  8. The Suitability of Orthogonal Hosts to Study Plant Cell Wall Biosynthesis. Pauly M, Gawenda N, Wagner C, Fischbach P, Ramírez V, Axmann IM, Voiniciuc C. Plants (Basel) 8 E516 (2019)
  9. Towards an understanding of the enzymatic degradation of complex plant mannan structures. Mafa MS, Malgas S. World J Microbiol Biotechnol 39 302 (2023)

Articles citing this publication (44)

  1. Glycan complexity dictates microbial resource allocation in the large intestine. Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Baslé A, Morland C, Day AM, Zheng H, Rogers TE, Thompson P, Hawkins AR, Yadav MP, Henrissat B, Martens EC, Dupree P, Gilbert HJ, Bolam DN. Nat Commun 6 7481 (2015)
  2. Galactomannan Catabolism Conferred by a Polysaccharide Utilization Locus of Bacteroides ovatus: ENZYME SYNERGY AND CRYSTAL STRUCTURE OF A β-MANNANASE. Bågenholm V, Reddy SK, Bouraoui H, Morrill J, Kulcinskaja E, Bahr CM, Aurelius O, Rogers T, Xiao Y, Logan DT, Martens EC, Koropatkin NM, Stålbrand H. J Biol Chem 292 229-243 (2017)
  3. Biochemical and mutational analyses of a multidomain cellulase/mannanase from Caldicellulosiruptor bescii. Su X, Mackie RI, Cann IK. Appl Environ Microbiol 78 2230-2240 (2012)
  4. Understanding how the complex molecular architecture of mannan-degrading hydrolases contributes to plant cell wall degradation. Zhang X, Rogowski A, Zhao L, Hahn MG, Avci U, Knox JP, Gilbert HJ. J Biol Chem 289 2002-2012 (2014)
  5. Comparative analyses of two thermophilic enzymes exhibiting both beta-1,4 mannosidic and beta-1,4 glucosidic cleavage activities from Caldanaerobius polysaccharolyticus. Han Y, Dodd D, Hespen CW, Ohene-Adjei S, Schroeder CM, Mackie RI, Cann IK. J Bacteriol 192 4111-4121 (2010)
  6. Tracing determinants of dual substrate specificity in glycoside hydrolase family 5. Chen Z, Friedland GD, Pereira JH, Reveco SA, Chan R, Park JI, Thelen MP, Adams PD, Arkin AP, Keasling JD, Blanch HW, Simmons BA, Sale KL, Chivian D, Chhabra SR. J Biol Chem 287 25335-25343 (2012)
  7. Molecular insights into substrate specificity and thermal stability of a bacterial GH5-CBM27 endo-1,4-β-D-mannanase. dos Santos CR, Paiva JH, Meza AN, Cota J, Alvarez TM, Ruller R, Ruller R, Prade RA, Squina FM, Murakami MT. J Struct Biol 177 469-476 (2012)
  8. Structural analysis of alkaline β-mannanase from alkaliphilic Bacillus sp. N16-5: implications for adaptation to alkaline conditions. Zhao Y, Zhang Y, Cao Y, Qi J, Mao L, Xue Y, Gao F, Peng H, Wang X, Gao GF, Ma Y. PLoS One 6 e14608 (2011)
  9. Novel β-1,4-Mannanase Belonging to a New Glycoside Hydrolase Family in Aspergillus nidulans. Shimizu M, Kaneko Y, Ishihara S, Mochizuki M, Sakai K, Yamada M, Murata S, Itoh E, Yamamoto T, Sugimura Y, Hirano T, Takaya N, Kobayashi T, Kato M. J Biol Chem 290 27914-27927 (2015)
  10. An Aspergillus nidulans β-mannanase with high transglycosylation capacity revealed through comparative studies within glycosidase family 5. Rosengren A, Reddy SK, Sjöberg JS, Aurelius O, Logan DT, Kolenová K, Stålbrand H. Appl Microbiol Biotechnol 98 10091-10104 (2014)
  11. Combined inhibitor free-energy landscape and structural analysis reports on the mannosidase conformational coordinate. Williams RJ, Iglesias-Fernández J, Stepper J, Jackson A, Thompson AJ, Lowe EC, White JM, Gilbert HJ, Rovira C, Davies GJ, Williams SJ. Angew Chem Int Ed Engl 53 1087-1091 (2014)
  12. Expression and characterization of a Bifidobacterium adolescentis beta-mannanase carrying mannan-binding and cell association motifs. Kulcinskaja E, Rosengren A, Ibrahim R, Kolenová K, Stålbrand H. Appl Environ Microbiol 79 133-140 (2013)
  13. Hydrolysis of konjac glucomannan by Trichoderma reesei mannanase and endoglucanases Cel7B and Cel5A for the production of glucomannooligosaccharides. Mikkelson A, Maaheimo H, Hakala TK. Carbohydr Res 372 60-68 (2013)
  14. Influence of a mannan binding family 32 carbohydrate binding module on the activity of the appended mannanase. Mizutani K, Fernandes VO, Karita S, Luís AS, Sakka M, Kimura T, Jackson A, Zhang X, Fontes CM, Gilbert HJ, Sakka K. Appl Environ Microbiol 78 4781-4787 (2012)
  15. β-mannanase (Man26A) and α-galactosidase (Aga27A) synergism - a key factor for the hydrolysis of galactomannan substrates. Malgas S, van Dyk SJ, Pletschke BI. Enzyme Microb Technol 70 1-8 (2015)
  16. An Aspergillus nidulans GH26 endo-β-mannanase with a novel degradation pattern on highly substituted galactomannans. von Freiesleben P, Spodsberg N, Blicher TH, Anderson L, Jørgensen H, Stålbrand H, Meyer AS, Krogh KB. Enzyme Microb Technol 83 68-77 (2016)
  17. Molecular dynamics study of enhanced Man5B enzymatic activity. Bernardi RC, Cann I, Schulten K. Biotechnol Biofuels 7 83 (2014)
  18. Molecular engineering of fungal GH5 and GH26 beta-(1,4)-mannanases toward improvement of enzyme activity. Couturier M, Féliu J, Bozonnet S, Roussel A, Berrin JG. PLoS One 8 e79800 (2013)
  19. Mannanase hydrolysis of spruce galactoglucomannan focusing on the influence of acetylation on enzymatic mannan degradation. Arnling Bååth J, Martínez-Abad A, Berglund J, Larsbrink J, Vilaplana F, Olsson L. Biotechnol Biofuels 11 114 (2018)
  20. Using Carbohydrate Interaction Assays to Reveal Novel Binding Sites in Carbohydrate Active Enzymes. Cockburn D, Wilkens C, Dilokpimol A, Nakai H, Lewińska A, Abou Hachem M, Svensson B. PLoS One 11 e0160112 (2016)
  21. Structural motif screening reveals a novel, conserved carbohydrate-binding surface in the pathogenesis-related protein PR-5d. Doxey AC, Cheng Z, Moffatt BA, McConkey BJ. BMC Struct Biol 10 23 (2010)
  22. Boosting of enzymatic softwood saccharification by fungal GH5 and GH26 endomannanases. von Freiesleben P, Spodsberg N, Stenbæk A, Stålbrand H, Krogh KBRM, Meyer AS. Biotechnol Biofuels 11 194 (2018)
  23. Endo-β-D-1,4-mannanase from Chrysonilia sitophila displays a novel loop arrangement for substrate selectivity. Gonçalves AM, Silva CS, Madeira TI, Coelho R, de Sanctis D, San Romão MV, Bento I. Acta Crystallogr D Biol Crystallogr 68 1468-1478 (2012)
  24. Enzymatic characterization of a glycoside hydrolase family 5 subfamily 7 (GH5_7) mannanase from Arabidopsis thaliana. Wang Y, Vilaplana F, Brumer H, Aspeborg H. Planta 239 653-665 (2014)
  25. Structural and functional analysis of a novel psychrophilic β-mannanase from Glaciozyma antarctica PI12. Parvizpour S, Razmara J, Ramli AN, Md Illias R, Shamsir MS. J Comput Aided Mol Des 28 685-698 (2014)
  26. The loop structure of Actinomycete glycoside hydrolase family 5 mannanases governs substrate recognition. Kumagai Y, Yamashita K, Tagami T, Uraji M, Wan K, Okuyama M, Yao M, Kimura A, Hatanaka T. FEBS J 282 4001-4014 (2015)
  27. A Novel Glycoside Hydrolase Family 113 Endo-β-1,4-Mannanase from Alicyclobacillus sp. Strain A4 and Insight into the Substrate Recognition and Catalytic Mechanism of This Family. Xia W, Lu H, Xia M, Cui Y, Bai Y, Qian L, Shi P, Luo H, Yao B. Appl Environ Microbiol 82 2718-2727 (2016)
  28. A surface-exposed GH26 β-mannanase from Bacteroides ovatus: Structure, role, and phylogenetic analysis of BoMan26B. Bågenholm V, Wiemann M, Reddy SK, Bhattacharya A, Rosengren A, Logan DT, Stålbrand H. J Biol Chem 294 9100-9117 (2019)
  29. Biochemical characterization of the novel endo-β-mannanase AtMan5-2 from Arabidopsis thaliana. Wang Y, Azhar S, Gandini R, Divne C, Ezcurra I, Aspeborg H. Plant Sci 241 151-163 (2015)
  30. Biochemical properties and atomic resolution structure of a proteolytically processed β-mannanase from cellulolytic Streptomyces sp. SirexAA-E. Takasuka TE, Acheson JF, Bianchetti CM, Prom BM, Bergeman LF, Book AJ, Currie CR, Fox BG. PLoS One 9 e94166 (2014)
  31. Cloning, Expression and Biochemical Characterization of Endomannanases from Thermobifida Species Isolated from Different Niches. Tóth Á, Barna T, Szabó E, Elek R, Hubert Á, Nagy I, Nagy I, Kriszt B, Táncsics A, Kukolya J. PLoS One 11 e0155769 (2016)
  32. Directed evolution of a family 26 glycoside hydrolase: endo-β-1, 4-mannanase from Pantoea agglomerans A021. Wang J, Zhang Q, Huang Z, Liu Z. J Biotechnol 167 350-356 (2013)
  33. Structure-based investigation into the functional roles of the extended loop and substrate-recognition sites in an endo-β-1,4-D-mannanase from the Antarctic springtail, Cryptopygus antarcticus. Kim MK, An YJ, Song JM, Jeong CS, Kang MH, Kwon KK, Lee YH, Cha SS. Proteins 82 3217-3223 (2014)
  34. Extent and Origins of Functional Diversity in a Subfamily of Glycoside Hydrolases. Glasgow EM, Vander Meulen KA, Takasuka TE, Bianchetti CM, Bergeman LF, Deutsch S, Fox BG. J Mol Biol 431 1217-1233 (2019)
  35. Mutational and structural analyses of Caldanaerobius polysaccharolyticus Man5B reveal novel active site residues for family 5 glycoside hydrolases. Oyama T, Schmitz GE, Dodd D, Han Y, Burnett A, Nagasawa N, Mackie RI, Nakamura H, Morikawa K, Cann I. PLoS One 8 e80448 (2013)
  36. Crystal structure and substrate interactions of an unusual fungal non-CBM carrying GH26 endo-β-mannanase from Yunnania penicillata. von Freiesleben P, Moroz OV, Blagova E, Wiemann M, Spodsberg N, Agger JW, Davies GJ, Wilson KS, Stålbrand H, Meyer AS, Krogh KBRM. Sci Rep 9 2266 (2019)
  37. Expression, homology modeling and enzymatic characterization of a new β-mannanase belonging to glycoside hydrolase family 1 from Enterobacter aerogenes B19. Liu S, Cui T, Song Y. Microb Cell Fact 19 142 (2020)
  38. NMR analysis of the binding mode of two fungal endo-β-1,4-mannanases from GH5 and GH26 families. Marchetti R, Berrin JG, Couturier M, Ul Qader SA, Molinaro A, Silipo A. Org Biomol Chem 14 314-322 (2016)
  39. Characterization of an inhibitor-resistant endo-1,4-β-mannanase from the gut microflora metagenome of Hermetia illucens. Song J, Kim SY, Kim DH, Lee YS, Sim JS, Hahn BS, Lee CM. Biotechnol Lett 40 1377-1387 (2018)
  40. Characterization of two GH5 endoglucanases from termite microbiome using synthetic metagenomics. Guerrero EB, de Villegas RMD, Soria MA, Santangelo MP, Campos E, Talia PM. Appl Microbiol Biotechnol 104 8351-8366 (2020)
  41. Exogenous β-mannanase improves feed conversion efficiency and reduces somatic cell count in dairy cattle. Tewoldebrhan TA, Appuhamy JADRN, Lee JJ, Niu M, Seo S, Jeong S, Kebreab E. J Dairy Sci 100 244-252 (2017)
  42. Impact of Modular Architecture on Activity of Glycoside Hydrolase Family 5 Subfamily 8 Mannanases. Møller MS. Molecules 27 1915 (2022)
  43. Marine bacteroidetes use a conserved enzymatic cascade to digest diatom β-mannan. Beidler I, Robb CS, Vidal-Melgosa S, Zühlke MK, Bartosik D, Solanki V, Markert S, Becher D, Schweder T, Hehemann JH. ISME J 17 276-285 (2023)
  44. Heterologous Expression of a Thermostable α-Galactosidase from Parageobacillus thermoglucosidasius Isolated from the Lignocellulolytic Microbial Consortium TMC7. Wang Y, Wang C, Chen Y, Cui M, Wang Q, Guo P. J Microbiol Biotechnol 32 749-760 (2022)


Quick links