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Functional Expression and Characterization of Acetyl Xylan Esterases CE Family 7 from Lactobacillus antri and Bacillus halodurans

  • Kim, Min-Jeong (Division of Animal, Horticultural and Food Sciences, Graduate School of Chungbuk National University) ;
  • Jang, Myoung-Uoon (Division of Animal, Horticultural and Food Sciences, Graduate School of Chungbuk National University) ;
  • Nam, Gyeong-Hwa (Division of Animal, Horticultural and Food Sciences, Graduate School of Chungbuk National University) ;
  • Shin, Heeji (Division of Animal, Horticultural and Food Sciences, Graduate School of Chungbuk National University) ;
  • Song, Jeong-Rok (Division of Animal, Horticultural and Food Sciences, Graduate School of Chungbuk National University) ;
  • Kim, Tae-Jip (Division of Animal, Horticultural and Food Sciences, Graduate School of Chungbuk National University)
  • Received : 2020.01.03
  • Accepted : 2020.01.15
  • Published : 2020.02.28

Abstract

Acetyl xylan esterase (AXE; E.C. 3.1.1.72) is one of the accessory enzymes for xylan degradation, which can remove the terminal acetate residues from xylan polymers. In this study, two genes encoding putative AXEs (LaAXE and BhAXE) were cloned from Lactobacillus antri DSM 16041 and Bacillus halodurans C-125, and constitutively expressed in Escherichia coli. They possess considerable activities towards various substrates such as p-nitrophenyl acetate, 4-methylumbelliferyl acetate, glucose pentaacetate, and 7-amino cephalosporanic acid. LaAXE and BhAXE showed the highest activities at pH 7.0 and 8.0 at 50℃, respectively. These enzymes are AXE members of carbohydrate esterase (CE) family 7 with the cephalosporine-C deacetylase activity for the production of antibiotics precursors. The simultaneous treatment of LaAXE with Thermotoga neapolitana β-xylanase showed 1.44-fold higher synergistic degradation of beechwood xylan than the single treatment of xylanase, whereas BhAXE showed no significant synergism. It was suggested that LaAXE can deacetylate beechwood xylan and enhance the successive accessibility of xylanase towards the resulting substrates. The novel LaAXE originated from a lactic acid bacterium will be utilized for the enzymatic production of D-xylose and xylooligosaccharides.

Keywords

References

  1. Huang YC, Chen GH, Chen YF, Chen WL, Yang CH. 2010. Heterologous expression of thermostable acetylxylan esterase gene from Thermobifida fusca and its synergistic action with xylanase for the production of xylooligosaccharides. Biochem. Biophys. Res. Commun. 400: 718-723. https://doi.org/10.1016/j.bbrc.2010.08.136
  2. Zheng F, Huang J, Yin Y, Ding S. 2013. A novel neutral xylanase with high SDS resistance from Volvariella volvacea: characterization and its synergistic hydrolysis of wheat bran with acetyl xylan esterase. J. Ind. Microbiol. Biotechnol. 40: 1083-1093. https://doi.org/10.1007/s10295-013-1312-4
  3. Hettiarachchi SA, Kwon YK, Lee Y, Jo E, Eom TY, Kang YH, et al. 2019. Characterization of an acetyl xylan esterase from the marine bacterium Ochrovirga pacifica and its synergism with xylanase on beechwood xylan. Microb. Cell Fact. 18: 122. https://doi.org/10.1186/s12934-019-1169-y
  4. Malgas S, Mafa MS, Mkabayi L, Pletschke B. 2019. A mini review of xylanolytic enzymes with regards to their synergistic interactions during hetero-xylan degradation. World J. Microbiol. Biotechnol. 35(12): 187. https://doi.org/10.1007/s11274-019-2765-z
  5. Biely P. 2012. Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol. Adv. 30: 1575-1588. https://doi.org/10.1016/j.biotechadv.2012.04.010
  6. Poeker SA, Geirnaert A, Berchtold L, Greppi A, Krych L, Steinert RE, et al. 2018. Understanding the prebiotic potential of different dietary fibers using an in vitro continuous adult fermentation model (PolyFermS). Sci. Rep. 8: 4318. https://doi.org/10.1038/s41598-018-22438-y
  7. Adesioye FA, Makhalanyane TP, Biely P, Cowan DA. 2016. Phylogeny, classification and metagenomic bioprospecting of microbial acetyl xylan esterases. Enzyme Microb. Technol. 93-94: 79-91. https://doi.org/10.1016/j.enzmictec.2016.07.001
  8. Sista Kameshwar AK, Qin W. 2018. Understanding the structural and functional properties of carbohydrate esterases with a special focus on hemicellulose deacetylating acetyl xylan esterases. Mycology 9: 273-295. https://doi.org/10.1080/21501203.2018.1492979
  9. Mitsushima K, Takimoto A, Sonoyama T, Yagi S. 1995. Gene cloning, nucleotide sequence, and expression of a cephalosporin-C deacetylase from Bacillus subtilis. Appl. Environ. Microbiol. 61: 2224-2229. https://doi.org/10.1128/aem.61.6.2224-2229.1995
  10. Degrassi G, Kojic M, Ljubijankic G, Venturi V. 2000. The acetyl xylan esterase of Bacillus pumilus belongs to a family of esterases with broad substrate specificity. Microbiology 146: 1585-1591. https://doi.org/10.1099/00221287-146-7-1585
  11. Levisson M, Han GW, Deller MC, Xu Q, Biely P, Hendriks S, et al. 2012. Functional and structural characterization of a thermostable acetyl esterase from Thermotoga maritima. Proteins 80: 1545-1559. https://doi.org/10.1002/prot.24041
  12. Tian Q, Song P, Jiang L, Li S, Huang H. 2014. A novel cephalosporin deacetylating acetyl xylan esterase from Bacillus subtilis with high activity toward cephalosporin C and 7-aminocephalosporanic acid. Appl. Microbiol. Biotechnol. 98: 2081-2089. https://doi.org/10.1007/s00253-013-5056-x
  13. Sonawane VC. 2006. Enzymatic modifications of cephalosporins by cephalosporin acylase and other enzymes. Crit. Rev. Biotechnol. 26: 95-120. https://doi.org/10.1080/07388550600718630
  14. Liu Y, Gong G, Zhu C, Zhu B, Hu Y. 2010. Environmentally safe production of 7-ACA by recombinant Acremonium chrysogenum. Curr. Microbiol. 61: 609-614. https://doi.org/10.1007/s00284-010-9660-z
  15. Viborg AH, Sorensen KI, Gilad O, Steen-Jensen DB, Dilokpimol A, Jacobsen S, et al. 2013. Biochemical and kinetic characterisation of a novel xylooligosaccharide-upregulated GH43 $\beta$-D-xylosidase/$\alpha$-L-arabinofuranosidase (BXA43) from the probiotic Bifidobacterium animalis s ubsp . lactis BB-12. AMB Express 3: 56. https://doi.org/10.1186/2191-0855-3-56
  16. Maria A, Margarita T, IIlia I, Iskra I. 2014. Gene expression of enzymes involved in utilization of xylooligosaccharides by Lactobacillus strains. Biotechnol. Biotechnol. Equip. 28: 941-948. https://doi.org/10.1080/13102818.2014.948257
  17. Park JM, Han NS, Kim TJ. 2007. Rapid detection and isolation of known and putative $\alpha$-L-arabinofuranosidase genes using degenerate PCR primers. J. Microbiol. Biotechnol. 17: 481-489.
  18. Khandeparker R, Jalal T. 2015. Xylanolytic enzyme systems in Arthrobacter sp. MTCC 5214 and Lactobacillus sp. Biotechnol. Appl. Biochem. 62: 245-254. https://doi.org/10.1002/bab.1253
  19. Roos S, Engstrand L, Jonsson H. 2005. Lactobacillus gastricus sp. nov., Lactobacillus antri sp. nov., Lactobacillus kalixensis sp. nov. and Lactobacillus ultunensis sp. nov., isolated from human stomach mucosa. Int. J. Syst. Evol. Microbiol. 55: 77-82. https://doi.org/10.1099/ijs.0.63083-0
  20. Takami H, Nakasone K, Takaki Y, Maeno G, Sasaki R, Masui N, et al. 2000. Complete genome sequence of the alkaliphilic bacterium Bacillus halodurans and genomic sequence comparison with Bacillus subtilis. Nucleic Acids Res. 28: 4317-4331. https://doi.org/10.1093/nar/28.21.4317
  21. Margolles-Clark E, Tenkanen M, Soderlund H, Penttila M. 1996. Acetyl xylan esterase from Trichoderma reesei contains an active-site serine residue and a cellulose-binding domain. Eur. J. Biochem. 237: 553-560. https://doi.org/10.1111/j.1432-1033.1996.0553p.x
  22. Koseki T, Miwa Y, Akao T, Akita O, Hashizume K. 2006. An Aspergillus oryzae acetyl xylan esterase: molecular cloning and characteristics of recombinant enzyme expressed in Pichia pastoris. J. Biotechnol. 121: 381-389. https://doi.org/10.1016/j.jbiotec.2005.07.015
  23. Krastanova I, Guarnaccia C, Zahariev S, Degrassi G, Lamba D. 2005. Heterologous expression, purification, crystallization, X-ray analysis and phasing of the acetyl xylan esterase from Bacillus pumilus. Biochim. Biophys. Acta 1748: 222-230. https://doi.org/10.1016/j.bbapap.2005.01.003
  24. Drzewiecki K, Angelov A, Ballschmiter M, Tiefenbach KJ, Sterner R, Liebl W. 2010. Hyperthermostable acetyl xylan esterase. Microb. Biotechnol. 3: 84-92. https://doi.org/10.1111/j.1751-7915.2009.00150.x
  25. Shao W, Wiegel J. 1995. Purification and characterization of two thermostable acetyl xylan esterases from Thermoanaerobacterium sp. strain JW/SL-YS485. Appl. Environ. Microbiol. 61: 729-733. https://doi.org/10.1128/aem.61.2.729-733.1995
  26. Yang CH, Liu WH. 2008. Purification and properties of an acetylxylan esterase from Thermobifida fusca. Enzyme Microb. Technol. 42: 181-186. https://doi.org/10.1016/j.enzmictec.2007.09.007
  27. Park SH, Yoo W, Lee CW, Jeong CS, Shin SC, Kim HW, et al. 2018. Crystal structure and functional characterization of a cold-active acetyl xylan esterase (PbAcE) from psychrophilic soil microbe Paenibacillus sp. PLoS One 13: e0206260. https://doi.org/10.1371/journal.pone.0206260
  28. Velikodvorskaya TV, Volkov IY, Vasilevko VT, Zverlov VV, Piruzian ES. 1997. Purification and some properties of Thermotoga neapolitana thermostable xylanase B expressed in E. coli cells. Biochemistry (Mosc) 62: 66-70.
  29. Vincent F, Charnock SJ, Verschueren KH, Turkenburg JP, Scott DJ, Offen WA, et al. 2003. Multifunctional xylooligosaccharide/cephalosporin C deacetylase revealed by the hexameric structure of the Bacillus subtilis enzyme at 1.9A resolution. J. Mol. Biol. 330: 593-606. https://doi.org/10.1016/S0022-2836(03)00632-6
  30. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10: 845-858. https://doi.org/10.1038/nprot.2015.053
  31. Singh M K, Manoj N . 2016. An extended loop in CE7 carbohydrate esterase family is dispensable for oligomerization but required for activity and thermostability. J. Struct. Biol. 194: 434-445. https://doi.org/10.1016/j.jsb.2016.04.008

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