Applied Microbiology and Biotechnology

, Volume 102, Issue 9, pp 3951–3965 | Cite as

The features that distinguish lichenases from other polysaccharide-hydrolyzing enzymes and the relevance of lichenases for biotechnological applications

  • Irina V. Goldenkova-Pavlova
  • Alexander А. Tyurin
  • Orkhan N. Mustafaev
Mini-Review
  • 78 Downloads

Abstract

The main specific features of β-1,3-1,4-glucanases (or lichenases, EC 3.2.1.73), the enzymes that in a strictly specific manner hydrolyze β-glucans of many cereal species and lichens containing β-1,3 and β-1,4 bonds, are reviewed as well as the current strategies used for their protein design, which have been successfully applied to make lichenases more attractive and promising for biocatalytic conversion of biomass, in particular, in the areas of their biotechnological application, such as brewing industry, animal feed manufacture, and biofuel production, which will in future allow these technologies to be economically and ecologically beneficial.

Keywords

Lichenase Properties Structure Stability Protein design Biotechnological application 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This work does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Addington T, Calisto B, Alfonso-Prieto M, Rovira C, Fita I, Planas A (2011) Re-engineering specificity in 1,3-1,4-β-glucanase to accept branched xyloglucan substrates. Proteins 79:365–375CrossRefPubMedGoogle Scholar
  2. Adeola O, Cowieson AJ (2011) Board-invited review: opportunities and challenges in using exogenous enzymes to improve nonruminant animal production. J Anim Sci 89(10):3189–3218.  https://doi.org/10.2527/jas.2010-3715 CrossRefPubMedGoogle Scholar
  3. Akinosho HO, Yoo CG, Dumitrache A, Natzke J, Muchero W, Brown SD, Ragauskas AJ (2017) Elucidating the structural changes to Populus lignin during consolidated bioprocessing with Clostridium thermocellum. ACS Sustain Chem Eng 5(9):7486–7491.  https://doi.org/10.1021/acssuschemeng.7b01203 CrossRefGoogle Scholar
  4. Amerah AM, van de Belt K, van Der Klis JD (2015) Effect of different levels of rapeseed meal and sunflower meal and enzyme combination on the performance, digesta viscosity and carcass traits of broiler chickens fed wheat-based diets. Animal 9(7):1131–1137.  https://doi.org/10.1017/S1751731115000142 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Aÿ J, Götz F, Borriss R, Heinemann U (1998) Structure and function of the Bacillus hybrid enzyme GluXyn-1: native-like jellyroll fold preserved after insertion of autonomous globular domain. Proc Natl Acad Sci 95(12):6613–6618.  https://doi.org/10.1073/pnas.95.12.6613 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bayer EA, Chanzy HR, Lamed R, Shoham Y (1998) Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol 8:548–557CrossRefPubMedGoogle Scholar
  7. Beckmann L, Simon O, Vahjen W (2006) Isolation and identification of mixed linked β-glucan degrading bacteria in the intestine of broiler chickens and partial characterization of respective 1,3-1,4-β-glucanase activities. J Basic Microbiol 46(3):175–185.  https://doi.org/10.1002/jobm.200510107 CrossRefPubMedGoogle Scholar
  8. Boisset C, Chanzy H, Henrissat B, Lamed R, Shoham Y, Bayer EA (1999) Digestion of crystalline cellulose substrates by the Clostridium thermocellum cellulosome: structural and morphological aspects. Biochem J 340:829–835CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burton RA, Fincher GB (2009) (1,3;1,4)-β-D-glucans in cell walls of the Poaceae, lower plants, and fungi: a tale of two linkages. Mol Plant 2:873–882CrossRefPubMedGoogle Scholar
  10. Celestino KR, Cunha RB, Felix CR (2006) Characterization of a beta-glucanase produced by Rhizopus microsporus var. microsporus, and its potential for application in the brewing industry. BMC Biochem 7:23.  https://doi.org/10.1186/1471-2091-7-23 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cerda LA, Valenzuela SV, Diaz P, Pastor FI (2016) New GH16 β-glucanase from Paenibacillus barcinonensis BP-23 releases a complex pattern of mixed-linkage oligomers from barley glucan. Biotechnol Appl Biochem 63(1):51–56.  https://doi.org/10.1002/bab.1348 CrossRefPubMedGoogle Scholar
  12. Chaari F, Belghith-Fendri L, Blibech M, Driss D, Ellouzi SZ, Sameh M, Chaabouni SE (2014) Biochemical characterization of a lichenase from Penicillium occitanis Pol6 and its potential application in the brewing industry. Process Biochem 49:1040–1046CrossRefGoogle Scholar
  13. Chen CC, Huang JW, Zhao P, Ko TP, Huang CH, Chan HC, Huang Z, Liu W, Cheng YS, Liu JR, Guo RT (2015) Structural analyses and yeast production of the beta-1,3-1,4-glucanase catalytic module encoded by the licB gene of Clostridium thermocellum. Enzym Microb Technol 71:1–7CrossRefGoogle Scholar
  14. Cheng YS, Huang CH, Chen CC, Huang TY, Ko TP, Huang JW, Wu TH, Liu JR, Guo RT (2014) Structural and mutagenetic analyses of a 1,3-1,4-β-glucanase from Paecilomyces thermophila. BBA Proteins Proteomics 1844(2):366–733.  https://doi.org/10.1016/j.bbapap.2013.11.005 CrossRefPubMedGoogle Scholar
  15. Cota J, Oliveira LC, Damásio AR, Citadini AP, Hoffmam ZB, Alvarez TM, Codima CA, Leite VB, Pastore G, de Oliveira-Neto M, Murakami MT, Ruller R, Ruller R, Squina FM (2013) Assembling a xylanase-lichenase chimera through all-atom molecular dynamics simulations. BBA Proteins Proteomics 1834:1492–1500.  https://doi.org/10.1016/j.bbapap.2013.02.030 CrossRefPubMedGoogle Scholar
  16. Debez A, Belghith I, Friesen J, Montzka C, Elleuche S (2017) Facing the challenge of sustainable bioenergy production: could halophytes be part of the solution? J Biol Eng 11:27CrossRefPubMedPubMedCentralGoogle Scholar
  17. Du R, Yan J, Li S, Zhang L, Zhang S, Li J, Zhao G, Qi P (2015) Cellulosic ethanol production by natural bacterial consortia is enhanced by Pseudoxanthomonas taiwanensis. Biotechnol Biofuels 8(1):10.  https://doi.org/10.1186/s13068-014-0186-7 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Elgharbi F, Ben Hlima H, Ameri R, Bejar S, Hmida-Sayari A (2017) A trimeric and thermostable lichenase from B. pumilus US570 strain: biochemical and molecular characterization. Int J Biol Macromol 95:273–280.  https://doi.org/10.1016/j.ijbiomac.2016.11.021 CrossRefPubMedGoogle Scholar
  19. Fu LL, Xu ZR, Shuai JB, Hu CX, Dai W, Li WF (2008) High-level secretion of a chimeric thermostable lichenase from Bacillus subtilis by screening of site-mutated signal peptides with structural alterations. Curr Microbiol 56(3):287–292.  https://doi.org/10.1007/s00284-007-9077-5 CrossRefPubMedGoogle Scholar
  20. Furtado GP, Ribeiro LF, Santos CR, Tonoli CC, Souza AR, Oliveira RR, Murakami MT, Ward RJ (2011) Biochemical and structural characterization of a β-1,3–1,4-glucanase from Bacillus subtilis 168. Process Biochem 46:1202–1206CrossRefGoogle Scholar
  21. Furtado GP, Ribeiro LF, Lourenzoni MR, Ward RJ (2013) A designed bifunctional laccase/β-1,3-1,4- glucanase enzyme shows synergistic sugar release from milled sugarcane bagasse. Protein Engineering Design and Selection 26 (1):15–23CrossRefGoogle Scholar
  22. Gilleran CT, Hernon AT, Murray PG, Tuohy MG (2010) Induction of enzyme cocktails by low cost carbon sources for production of monosaccharide-rich syrups from plant materials. Bioresources 5(2):634–649Google Scholar
  23. Guan LZ, Sun YP, Xi QY, Wang JL, Zhou JY, Shu G, Jiang QY, Zhang YL (2013) β-Glucanase specific expression in the parotid gland of transgenic mice. Transgenic Res 22(4):805–812.  https://doi.org/10.1007/s11248-012-9682-3 CrossRefPubMedGoogle Scholar
  24. Guan LZ, Cai JS, Zhao S, Sun YP, Wang JL, Jiang Y, Shu G, Jiang QY, Wu ZF, Xi QY, Zhang YL (2017) Improvement of anti-nutritional effect resulting from β-glucanase specific expression in the parotid gland of transgenic pigs. Transgenic Res 26(1):1–11.  https://doi.org/10.1007/s11248-016-9984-y CrossRefPubMedGoogle Scholar
  25. Hahn M, Piotukh K, Borriss R, Heinemann U (1994) Native-like in vivo folding of a circularly permuted jellyroll protein shown by crystal structure analysis. Proc Natl Acad Sci U S A 91:10417–10421CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hahn M, Pons J, Planas A, Querol E, Heinemann U (1995) Crystal structure of Bacillus licheniformis 1,3-1,4-beta-D-glucan 4-glucanohydrolase at 1.8 A resolution. FEBS Lett 374:221–224CrossRefPubMedGoogle Scholar
  27. Heinemann U, Hahn M (1995) Circular permutation of polypeptide chains: implications for protein folding and stability. Prog Biophys Mol Biol 64(2/3):121–143CrossRefPubMedGoogle Scholar
  28. Huang JW, Cheng YS, Ko TP, Lin CY, Lai HL, Chen CC, Ma Y, Zheng Y, Huang CH, Zou P, Liu JR, Guo RT (2012) Rational design to improve thermostability and specific activity of the truncated Fibrobacter succinogenes 1,3-1,4-β-D-glucanase. Appl Microbiol Biotechnol 94(1):111–121.  https://doi.org/10.1007/s00253-011-3586-7 CrossRefPubMedGoogle Scholar
  29. Iakiviak M, Mackie R, Cann IK (2011) Functional analyses of multiple lichenin-degrading enzymes from the rumen bacterium Ruminococcus albus 8. Appl Environ Microbiol 77(21):7541–7450.  https://doi.org/10.1128/AEM.06088-11 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Józefiak D, Rutkowski A, Jensen BB, Engberg RM (2006) The effect of beta-glucanase supplementation of barley- and oat-based diets on growth performance and fermentation in broiler chicken gastrointestinal tract. Br Poult Sci 47(1):57–64CrossRefPubMedGoogle Scholar
  31. Keitel T, Simon O, Borriss R, Heinemann U (1993) Molecular and active-site structure of a Bacillus 1,3–1,4-betaglucanase. Proceedings of the National Academy of Sciences 90 (11):5287–5291CrossRefGoogle Scholar
  32. Kim JY (2003) Overproduction and secretion of Bacillus circulans endo-beta-1,3-1,4-glucanase gene (bglBC1) in B. subtilis and B. megaterium. Biotechnol Lett 25(17):1445–1449CrossRefPubMedGoogle Scholar
  33. Kim KH, Kim YO, Ko BS, Youn HJ, Lee DS (2004) Over-expression of the gene (bglBC1) from Bacillus circulans encoding an endo-beta-(1-->3),(1-->4)-glucanase useful for the preparation of oligosaccharides from barley beta-glucan. Biotechnol Lett 26(22):1749–1755CrossRefPubMedGoogle Scholar
  34. Kim YR, Kim EY, Lee JM, Kim JK, Kong IS (2013) Characterisation of a novel Bacillus sp. SJ-10 β-1,3-1,4-glucanase isolated from jeotgal, a traditional Korean fermented fish. Bioprocess Biosyst Eng 36:721–727CrossRefPubMedGoogle Scholar
  35. Kumar R, Singh S, Singh OV (2008) Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J Ind Microbiol Biotechnol 35:377–391CrossRefPubMedGoogle Scholar
  36. Lewis MJ, TWY (2013) Brewing. Springer, New YorkGoogle Scholar
  37. Linton SM, Greenaway P (2004) Presence and properties of cellulase and hemicellulase enzymes of the gecarcinid land crabs Gecarcoidea natalis and Discoplax hirtipes. J Exp Biol 207:4095–4104CrossRefPubMedGoogle Scholar
  38. Liu WC, Lin YS, Jeng WY, Chen JH, Wang AH, Shyur LF (2012) Engineering of dual-functional hybrid glucanases. Protein Eng Des Sel 25(11):771–780.  https://doi.org/10.1093/protein/gzs083 CrossRefPubMedGoogle Scholar
  39. Liu D, Li J, Zhao S, Zhang R, Wang M, Miao Y, Shen Y, Shen Q (2013) Secretome diversity and quantitative analysis of cellulolytic Aspergillus fumigatus Z5 in the presence of different carbon sources. Biotechnol for Biofuels 6(1):149.  https://doi.org/10.1186/1754-6834-6-149 CrossRefGoogle Scholar
  40. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495.  https://doi.org/10.1093/nar/gkt1178 CrossRefPubMedGoogle Scholar
  41. Louw ME, Reid SJ, Watson TG (1993) Characterization, cloning and sequencing of a thermostable endo-(1,3-1,4) beta-glucanase-encoding gene from an alkalophilic Bacillus brevis. Appl Microbiol Biotechnol 38(4):507–513CrossRefPubMedGoogle Scholar
  42. Luo Z, Gao Q, Li X, Bao J (2014) Cloning of LicB from Clostridium thermocellum and its efficient secretive expression of thermostable β-1,3-1,4-glucanase. Appl Biochem Biotechnol 173:562–570.  https://doi.org/10.1007/s12010-014-0863-9. CrossRefPubMedGoogle Scholar
  43. Manavalan A, Adav SS, Sze SK (2011) iTRAQ-based quantitative secretome analysis of Phanerochaete chrysosporium. J Proteomics 75:642–654CrossRefPubMedGoogle Scholar
  44. Mao S, Lu Z, Zhang C, Lu F, Bie X (2013) Purification, characterization, and heterologous expression of a thermostable β-1,3-1,4-glucanase from Bacillus altitudinis YC-9. Appl Biochem Biotechnol 169:960–975CrossRefPubMedGoogle Scholar
  45. Masilamani R, Sharma OP, Muthuvel SK, Natarajan S (2013) Cloning, expression of β-1,3-1,4 glucanase from Bacillus subtilis SU40 and the effect of calcium ion on the stability of recombinant enzyme: in vitro and in silico analysis. Bioinformation 9(19):958–962.  https://doi.org/10.6026/97320630009958.eCollection2013. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Menon V, Divate R, Rao M (2011) Bioethanol production from renewable polymer lichenan using lichenase from an alkalothermophilic Thermomonospora sp. and thermotolerant yeast. Fuel Process Technol 92:401–406CrossRefGoogle Scholar
  47. Musiychuk K, Stephenson N, Bi H, Farrance CE, Orozovic G, Brodelius M, Brodelius P, Horsey A, Ugulava N, Shamloul AM, Mett V, Rabindran S, Streatfield SJ, Yusibov V (2007) A launch vector for the production of vaccine antigens in plants. Influenza Other Respir Viruses 1:19–25.  https://doi.org/10.1111/j.1750-2659.2006.00005.x CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nghiem NP, Brooks WS, Griffey CA, Toht MJ (2017) Production of ethanol from newly developed and improved winter barley cultivars. Appl Biochem Biotechnol 82(1):400–410.  https://doi.org/10.1007/s12010-016-2334-y CrossRefGoogle Scholar
  49. Niu C, Zhu L, Wang J, Li Q (2014) Simultaneous enhanced catalytic activity and thermostability of a 1,3-1,4-β-glucanase from Bacillus amyloliqueformis by chemical modification of lysine residues. Biotechnol Lett 36(12):2453–2460.  https://doi.org/10.1007/s10529-014-1616-0 Epub 2014 Jul 22CrossRefPubMedGoogle Scholar
  50. Niu Q, Zhang G, Zhang L, Ma Y, Shi Q, Fu W (2016a) Purification and characterization of a thermophilic 1,3-1,4-β-glucanase from Bacillus methylotrophicus S2 isolated from booklice. J Biosci Bioeng 121(5):503–508.  https://doi.org/10.1016/j.jbiosc.2015.10.007 Epub 2015 Nov 14CrossRefPubMedGoogle Scholar
  51. Niu C, Zhu L, Xu X, Li Q (2016b) Rational design of disulfide bonds increases thermostability of a mesophilic 1,3-1,4-β-glucanase from Bacillus terquilensis. PLoS One 11(4):e0154036.  https://doi.org/10.1371/journal.pone.0154036 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Niu C, Liu C, Li Y, Zheng F, Wang J, Li Q (2018) Production of a thermostable 1,3-1,4-β-glucanase mutant in Bacillus subtilis WB600 at a high fermentation capacity and its potential application in the brewing industry. Int J Biol Macromol 107(Pt A):28–34.  https://doi.org/10.1016/j.ijbiomac.2017.08.139 CrossRefPubMedGoogle Scholar
  53. Olgun O, Altay Y, Yildiz AO. (2018) Effects of carbohydrase enzyme supplementation on performance, eggshell quality, and bone parameters of laying hens fed on maize- and wheat-based diets. Br Poult Sci 1–7.  https://doi.org/10.1080/00071668.2018.1423677
  54. Olsen O, Thomsen KK, Weber J, Duus JO, Svendsen I, Wegener C, von Wettstein D (1996) Transplanting two unique beta-glucanase catalytic activities into one multienzyme, which forms glucose. Biotechnology (NY) 14(1):71–76Google Scholar
  55. Pagliano G, Ventorino V, Panico A, Pepe O (2017) Integrated systems for biopolymers and bioenergy production from organic waste and by-products: a review of microbial processes. Biotechnol Biofuels 10:113.  https://doi.org/10.1186/s13068-017-0802-4; CrossRefPubMedPubMedCentralGoogle Scholar
  56. Papanek B, Biswas R, Rydzak T, Guss AM (2015) Elimination of metabolic pathways to all traditional fermentation products increases ethanol yields in Clostridium thermocellum. Metab Eng 32:49–54CrossRefPubMedGoogle Scholar
  57. Pauly M, Keegstra K (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J 54:559–568CrossRefPubMedGoogle Scholar
  58. Pei H, Guo X, Yang W, Lv J, Chen Y, Cao Y (2015) Directed evolution of a β-1,3-1,4-glucanase from Bacillus subtilis MA139 for improving thermal stability and other characteristics. J Basic Microbiol 55(7):869–878.  https://doi.org/10.1002/jobm.201400664 CrossRefPubMedGoogle Scholar
  59. Piruzian ES, Goldenkova IV, Musiychuk KA, Kobets NS, Arman IP, Bobrysheva IV, Chekhuta IA, Glazkova D (2002) A reporter system for prokaryotic and eukaryotic cells based on thermostable Clostridium thermocellum lichenase. Mol Gen Genomics 266:778–786.  https://doi.org/10.1007/s00438-001-0595-8 CrossRefGoogle Scholar
  60. Planas A (2000) Bacterial 1,3-1,4-L-glucanases: structure, function and protein engineering. Biochim Biophys Acta 1543:361–382CrossRefPubMedGoogle Scholar
  61. Qiao J, Dong B, Li Y, Zhang B, Cao Y (2009) Cloning of a β-1,3-1,4-glucanase gene from Bacillus subtilis MA139 and its functional expression in Escherichia coli. Appl Biochem Biotechnol 152:334–342CrossRefPubMedGoogle Scholar
  62. Rao VH, Gosavi S (2014) In the multi-domain protein adenylate kinase, domain insertion facilitates cooperative folding while accommodating function at domain interfaces. PLoS Comput Biol 10(11):e1003938CrossRefGoogle Scholar
  63. Ribeiro LF, Furtado GP, Lourenzoni MR, Costa-Filho AJ, Santos CR, Nogueira SC, Betini JA, Polizeli Mde L, Murakami MT, Ward RJ (2011) Engineering bifunctional laccase-xylanase chimeras for improved catalytic performance. J Biol Chem 286(50):43026–43038.  https://doi.org/10.1074/jbc.M111.253419 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ribeiro T, Lordelo MM, Prates JA, Falcão L, Freire JP, Ferreira LM, Fontes CM (2012) The thermostable β-1,3-1,4-glucanase from Clostridium thermocellum improves the nutritive value of highly viscous barley-based diets for broilers. Br Poult Sci 53(2):224–234.  https://doi.org/10.1080/00071668.2012.674632 CrossRefPubMedGoogle Scholar
  65. Ribeiro LF, Lourenzoni MR, Ward RJ (2013) A designed bifunctional laccase/β-1,3-1,4-glucanase enzyme shows synergistic sugar release from milled sugarcane bagasse. Protein Eng Des Sel 26(1):15–23.  https://doi.org/10.1093/protein/gzs057 CrossRefPubMedGoogle Scholar
  66. Scanes CG, Brant G, Ensminger ME (2004) Poultry science. Pearson Prentice Hall, Upper Saddle RiverGoogle Scholar
  67. Schimming S, Schwarz WH, Staudenbauer WL (1991) Properties of a thermoactive beta-1,3-1,4-glucanase (lichenase) from Clostridium thermocellum expressed in Escherichia coli. Biochem Biophys Res Commun 177(1):447–452CrossRefPubMedGoogle Scholar
  68. Solomon KV, Haitjema CH, Henske JK, Gilmore SP, Borges-Rivera D, Lipzen A, Brewer HM, Purvine SO, Wright AT, Theodorou MK, Grigoriev IV, Regev A, Thompson DA, O'Malley MA (2016) Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes. Science 351(6278):1192–1195.  https://doi.org/10.1126/science.aad1431 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Spilliaert R, Hreggvidsson GO, Kristjansson JK, Eggertsson G, Palsdottir A (1994) Cloning and sequencing of a Rhodothermus marinus gene, bglA, coding for a thermostable beta-glucanase and its expression in Escherichia coli. Eur J Biochem 224(3):923–930CrossRefPubMedGoogle Scholar
  70. Sun J, Li W, Gu S (2002) Stability of beta glucanase under conditions simulating animal digestive tract in vitro. Chin J Anim Sci 38:18–19Google Scholar
  71. Sun J, Wang H, Lv W, Ma C, Lou Z, Dai Y (2011) Construction and characterization of a fusion β-1,3-1,4-glucanase to improve hydrolytic activity and thermostability. Biotechnol Lett 33(11):2193–2199.  https://doi.org/10.1007/s10529-011-0676-7 CrossRefPubMedGoogle Scholar
  72. Susenbeth A, Naatjes M, Blank B, Kühl R, Ader P, Dickhoefer U (2011) Effect of xylanase and glucanase supplementation to a cereal-based, threonine-limited diet on the nitrogen balance of growing pigs. Arch Anim Nutr 65(2):123–133CrossRefPubMedGoogle Scholar
  73. Tabernero C, Coll PM, Fernández-Abalos JM, Pérez P, Santamaría RI (1994) Cloning and DNA sequencing of bgaA, a gene encoding an endo-beta-1,3-1,4-glucanase, from an alkalophilic Bacillus strain (N137). Appl Environ Microbiol 60(4):1213–1220PubMedPubMedCentralGoogle Scholar
  74. Tang Y, Yang S, Yan Q, Zhou P, Cui J, Jiang Z (2012) Purification and characterization of a novel β-1,3−1,4-glucanase (lichenase) from thermophilic Rhizomucor miehei with high specific activity and its gene sequence. J Agric Food Chem 60:2354–2361CrossRefPubMedGoogle Scholar
  75. Teng D, Wang JH, Fan Y, Yang YL, Tian ZG, Luo J, Yang GP, Zhang F (2006) Cloning of β-1,3-1,4-glucanase gene from Bacillus licheniformis EGW039 (CGMCC 0635) and its expression in Escherichia coli BL21 (DE3). Appl Microbiol Biotechnol 72:705–712.  https://doi.org/10.1007/s00253-006-0329-2 CrossRefPubMedGoogle Scholar
  76. Teng D, Fan Y, Yang YL, Tian ZG, Luo J, Wang JH (2007) Codon optimization of Bacillus licheniformis beta-1,3-1,4-glucanase gene and its expression in Pichia pastoris. Appl Microbiol Biotechnol 74(5):1074–1083 Epub 2007 Jan 11CrossRefPubMedGoogle Scholar
  77. Tsai LC, Shyur LF, Lee SH, Lin SS, Yuan HS (2003) Crystal structure of a natural circularly permuted jellyroll protein: 1,3-1,4-beta-D-glucanase from Fibrobacter succinogenes. J Mol Biol 330:607–620CrossRefPubMedGoogle Scholar
  78. Tsuji A, Tominaga K, Nishiyama N, Yuasa K (2013) Comprehensive enzymatic analysis of the cellulolytic system in digestive fluid of the sea hare Aplysia kurodai. Efficient glucose release from sea lettuce by synergistic action of 45 kDa endoglucanase and 210 kDa ß-glucosidase. PLoS One 8(6):e65418.  https://doi.org/10.1371/journal.pone.0065418 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Tyurin АА, Sadovskaya NS, Nikiforova KR, Mustafaev ОN, Komakhin RA, Fadeev VS, Goldenkova-Pavlova IV (2015) Clostridium thermocellum thermostable lichenase with circular permutations and modifications in the N-terminal region retains its activity and thermostability. BBA - Proteins and Proteomics 1854(1):10–19.  https://doi.org/10.1016/j.bbapap.2014.10.012 CrossRefGoogle Scholar
  80. Tyurin АА, Kabardaeva KV, Mustafaev ОN, Pavlenko ОS, Sadovskaya NS, Fadeev VS, Zvonova ЕА, Goldenkova-Pavlova IV (2018) Expression of soluble and active interferon α-A in periplasm Escherichia coli by fusion with thermostable lichenase using the domain insertion approach. Biochem Mosc 83(3):259–269Google Scholar
  81. van Rensburg P, van Zyl WH, Pretorius IS (1997) Over-expression of the Saccharomyces cerevisiae exo-beta-1,3-glucanase gene together with the Bacillus subtilis endo-beta-1,3-1,4-glucanase gene and the Butyrivibrio fibrisolvens endo-beta-1,4-glucanase gene in yeast. J Biotechnol 55 (1):43–53CrossRefPubMedGoogle Scholar
  82. Viladot JL, Canals F, Batllori X, Planas A (2001) Long-lived glycosyl-enzyme intermediate mimic produced by formate re-activation of a mutant endoglucanase lacking its catalytic nucleophile. Biochem J 355:79–86CrossRefPubMedPubMedCentralGoogle Scholar
  83. Von Wettstein D, Warner J, Kannangara CG (2003) Supplements of transgenic malt or grain containing (1,3-1,4)-beta-glucanase increase the nutritive value of barley-based broiler diets to that of maize. Br Poult Sci 44(3):438–449CrossRefGoogle Scholar
  84. Wang J, Niu C, Liu X, Chen X, Li Q (2014) Characterization of a new 1,3-1,4-β-glucanase gene from Bacillus tequilensis CGX5-1. Appl Biochem Biotechnol 173(3):826–837.  https://doi.org/10.1007/s12010-014-0900-8 CrossRefPubMedGoogle Scholar
  85. Wang J, Wang Y, Wang X, Zhang D, Wu S, Zhang G (2016) Enhanced thermal stability of lichenase from Bacillus subtilis 168 by SpyTag/SpyCatcher-mediated spontaneous cyclization. Biotechnol Biofuels. 9:79.  https://doi.org/10.1186/s13068-016-0490-5 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Wang X, Ge H, Zhang D, Wu S, Zhang G (2017) Oligomerization triggered by foldon: a simple method to enhance the catalytic efficiency of lichenase and xylanase. BMC Biotechnol 17:57.  https://doi.org/10.1186/s12896-017-0380-3 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Wen TN, Chen JL, Lee SH, Yang NS, Shyur LF (2005) A truncated Fibrobacter succinogenes 1,3-1,4-beta-d-glucanase with improved enzymatic activity and thermotolerance. Biochemistry 44(25):9197–2905CrossRefPubMedGoogle Scholar
  88. Wilson CM, Rodriguez M Jr, Johnson CM, Martin SL, Chu TM, Wolfinger RD, Hauser LJ, Land ML, Klingeman DM, Syed MH, Ragauskas AJ, Tschaplinski TJ, Mielenz JR, Brown SD (2013) Global transcriptome analysis of Clostridium thermocellum ATCC 27405 during growth on dilute acid pretreated Populus and switchgrass. Biotechnol Biofuels. 6(1):179.  https://doi.org/10.1186/1754-6834-6-179 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Xu T, Zhu T, Li S (2016) β-1,3–1,4-glucanase gene from Bacillus velezensis ZJ20 exerts antifungal effect on plant pathogenic fungi. World J Microbiol Biotechnol 32(2):26.  https://doi.org/10.1007/s11274-015-1985-0 CrossRefPubMedGoogle Scholar
  90. Yang SQ, Xiong H, Yang HY, Yan QJ, Jiang ZQ (2014) High-level production of β-1,3-1,4-glucanase by Rhizomucor miehei under solid-state fermentation and its potential application in the brewing industry. J Appl Microbiol 118:84–91CrossRefPubMedGoogle Scholar
  91. Zhang Q, Chen Q, Fu M, Wang J, Zhang H, He G (2008) Construction of recombinant industrial Saccharomyces cerevisiae strain with bglS gene insertion into PEP4 locus by homologous recombination. J Zhejiang Univ Sci B 9(7):527–535CrossRefPubMedPubMedCentralGoogle Scholar
  92. Zhang L, Zhao P, Chen CC, Huang CH, Ko TP, Zheng Y, Guo RT (2014) Preliminary X-ray diffraction analysis of a thermophilic β-1,3–1,4-glucanase from Clostridium thermocellum. Acta Cryst F70:946–948Google Scholar
  93. Zhang J, Gao Y, Lu Q, Sa R, Zhang H (2017a) Proteome changes in the small intestinal mucosa of growing pigs with dietary supplementation of non-starch polysaccharide enzymes. Proteome Sci 15:3CrossRefPubMedPubMedCentralGoogle Scholar
  94. Zhang B, Liu Y, Yang H, Yan Q, Yang S, Jiang ZQ, Li S (2017b) Biochemical properties and application of a novel β-1,3-1,4-glucanase from Paenibacillus barengoltzii. Food Chem 234:68–75.  https://doi.org/10.1016/j.foodchem.2017.04.162 CrossRefPubMedGoogle Scholar
  95. Zverlov VV, Schwarz WH (2008) Bacterial cellulose hydrolysis in anaerobic environmental subsystems—Clostridium thermocellum and Clostridium stercorarium, thermophilic plant-fiber degraders. Ann N Y Acad Sci 1125:298–307.  https://doi.org/10.1196/annals.1419.008 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Irina V. Goldenkova-Pavlova
    • 1
    • 2
  • Alexander А. Tyurin
    • 1
    • 2
  • Orkhan N. Mustafaev
    • 3
  1. 1.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Department of Genetics and BiotechnologyRussian State Agrarian University–Moscow Timiryazev Agricultural AcademyMoscowRussia
  3. 3.Department of Biophysics and Molecular BiologyBaku State UniversityBakuAzerbaijan

Personalised recommendations