Login Register Cart 0
Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Production and Functional Characterization of a Novel Mannanase from Alteromonadaceae Bacterium Bs31

Author(s): Rui Ding, Huifang Xie, Zhenggang Han* and Jiangke Yang

Volume 29, Issue 8, 2022

Published on: 10 August, 2022

Page: [692 - 701] Pages: 10

DOI: 10.2174/0929866529666220615161603

Price: $65

Abstract

Background: Mannans are the main components of hemicellulose in nature and serve as the major storage polysaccharide in legume seeds. To mine new mannanase genes and identify their functional characteristics are an important basis for mannan biotechnological applications.

Objective: In this study, a putative mannanase gene (ManBs31) from the genome of the marine bacterium Alteromonadaceae Bs31 was characterized.

Methods: Amino acid sequence analysis and protein structural modeling were used to reveal the molecular features of ManBs31. The catalytic domain of ManBs31 was recombinantly produced using Escherichia coli and Pichia pastoris expression systems. The biochemical properties of the enzymes were determined by reducing sugar assay and thin-layer chromatography.

Results: Sequence analysis revealed that ManBs31 was a multidomain protein, consisting of a catalytic domain belonging to glycoside hydrolase family 5 (GH5) and two cellulose-binding domains. Recombinant ManBs31-GH5 exhibited the maximum hydrolytic performance at 70 ºC and pH 6. It showed the best hydrolysis capacity toward konjac glucomannan (specific enzyme activity up to 1070.84 U/mg) and poor hydrolysis ability toward galactomannan with high side-chain modifications (with a specific activity of 344.97 U/mg and 93.84 U/mg to locust bean gum and ivory nut mannan, respectively). The hydrolysis products of ManBs31-GH5 were mannooligosaccharides, and no monosaccharide was generated. Structural analysis suggested that ManBs31-GH5 had a noncanonical +2 subsite compared with other GH5 mannanases.

Conclusion: ManBs31 was a novel thermophilic endo-mannanase and it provided a new alternative for the biodegradation of mannans, especially for preparation of probiotic mannooligosaccharides.

Keywords: Auto-induction, Escherichia coli expression, glycoside hydrolase family 5, mannanase, mannooligosaccharides, Pichia pastoris expression.

« Previous Next »
Graphical Abstract

[1]
Scheller, H.V.; Ulvskov, P. Hemicelluloses. Annu. Rev. Plant Biol., 2010, 61(1), 263-289.
[http://dx.doi.org/10.1146/annurev-arplant-042809-112315] [PMID: 20192742]
[2]
Moreira, L.R.; Filho, E.X. An overview of mannan structure and mannan-degrading enzyme systems. Appl. Microbiol. Biotechnol., 2008, 79(2), 165-178.
[http://dx.doi.org/10.1007/s00253-008-1423-4] [PMID: 18385995]
[3]
Srivastava, P.K.; Kapoor, M. Production, properties, and applications of endo-β-mannanases. Biotechnol. Adv., 2017, 35(1), 1-19.
[http://dx.doi.org/10.1016/j.biotechadv.2016.11.001] [PMID: 27836790]
[4]
Dawood, A.; Ma, K. Applications of microbial β-mannanases. Front. Bioeng. Biotechnol., 2020, 8, 598630.
[http://dx.doi.org/10.3389/fbioe.2020.598630] [PMID: 33384989]
[5]
Tewoldebrhan, T.A.; Appuhamy, J.A.D.R.N.; Lee, J.J.; Niu, M.; Seo, S.; Jeong, S.; Kebreab, E. Exogenous β-mannanase improves feed conversion efficiency and reduces somatic cell count in dairy cattle. J. Dairy Sci., 2017, 100(1), 244-252.
[http://dx.doi.org/10.3168/jds.2016-11017] [PMID: 28341045]
[6]
Latham, R.E.; Williams, M.P.; Walters, H.G.; Carter, B.; Lee, J.T. Efficacy of β-mannanase on broiler growth performance and energy utilization in the presence of increasing dietary galactomannan. Poult. Sci., 2018, 97(2), 549-556.
[http://dx.doi.org/10.3382/ps/pex309] [PMID: 29121338]
[7]
Singh, S.; Singh, G.; Khatri, M.; Kaur, A.; Arya, S.K. Thermo and alkali stable β-mannanase: Characterization and application for removal of food (mannans based) stain. Int. J. Biol. Macromol., 2019, 134, 536-546.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.05.067] [PMID: 31100392]
[8]
David, A.; Singh Chauhan, P.; Kumar, A.; Angural, S.; Kumar, D.; Puri, N.; Gupta, N. Coproduction of protease and mannanase from Bacillus nealsonii PN-11 in solid state fermentation and their combined application as detergent additives. Int. J. Biol. Macromol., 2018, 108, 1176-1184.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.09.037] [PMID: 28919530]
[9]
Panwar, D.; Kapoor, M. Transcriptional analysis of galactomannooligosaccharides utilization by Lactobacillus plantarum WCFS1. Food Microbiol., 2020, 86, 103336.
[http://dx.doi.org/10.1016/j.fm.2019.103336] [PMID: 31703861]
[10]
Wei, X.; Fu, X.; Xiao, M.; Liu, Z.; Zhang, L.; Mou, H. Dietary galactosyl and mannosyl carbohydrates: In-vitro assessment of prebiotic effects. Food Chem., 2020, 329, 127179.
[http://dx.doi.org/10.1016/j.foodchem.2020.127179] [PMID: 32505987]
[11]
Cho, S.S.; Choi, Y.H.; Choi, Y.S.; Jee, J.P.; Seong, C.N.; Yoo, J.C.; Pradeep, G.C. An extremely alkaline mannanase from Streptomyces sp. CS428 hydrolyzes galactomannan producing series of mannooligosaccharides. World J. Microbiol. Biotechnol., 2016, 32(5), 84.
[http://dx.doi.org/10.1007/s11274-016-2040-5] [PMID: 27038954]
[12]
Kaira, G.S.; Kapoor, M. Molecular advancements on over-expression, stability and catalytic aspects of endo-β-mannanases. Crit. Rev. Biotechnol., 2021, 41(1), 1-15.
[http://dx.doi.org/10.1080/07388551.2020.1825320] [PMID: 33032458]
[13]
Soni, H.; Kango, N. Hemicellulases in lignocellulose biotechnology. Recent Pat. Biotechnol., 2013, 7(3), 207-218.
[http://dx.doi.org/10.2174/18722083113076660011] [PMID: 24182321]
[14]
Yamabhai, M.; Sak-Ubol, S.; Srila, W.; Haltrich, D. Mannan biotechnology: From biofuels to health. Crit. Rev. Biotechnol., 2016, 36(1), 32-42.
[http://dx.doi.org/10.3109/07388551.2014.923372] [PMID: 25025271]
[15]
Goyal, D.; Kumar, K.; Centeno, M.S.J.; Thakur, A.; Pires, V.M.R.; Bule, P.; Fontes, C.M.G.A.; Goyal, A. Molecular cloning, expression and biochemical characterization of a family 5 glycoside hydrolase first endo-mannanase (RfGH5_7) from Ruminococcus flavefaciens FD-1 v3. Mol. Biotechnol., 2019, 61(11), 826-835.
[http://dx.doi.org/10.1007/s12033-019-00205-2] [PMID: 31435842]
[16]
Liao, H.; Li, S.; Zheng, H.; Wei, Z.; Liu, D.; Raza, W.; Shen, Q.; Xu, Y. A new acidophilic thermostable endo-1,4-β-mannanase from Penicillium oxalicum GZ-2: Cloning, characterization and functional expression in Pichia pastoris. BMC Biotechnol., 2014, 14(1), 90.
[http://dx.doi.org/10.1186/s12896-014-0090-z] [PMID: 25348022]
[17]
Zang, H.; Xie, S.; Wu, H.; Wang, W.; Shao, X.; Wu, L.; Rajer, F.U.; Gao, X. A novel thermostable GH5_7 β-mannanase from Bacillus pumilus GBSW19 and its application in Manno-Oligosaccharides (MOS) production. Enzyme Microb. Technol., 2015, 78, 1-9.
[http://dx.doi.org/10.1016/j.enzmictec.2015.06.007] [PMID: 26215338]
[18]
Seesom, W.; Thongket, P.; Yamamoto, T.; Takenaka, S.; Sakamoto, T.; Sukhumsirichart, W. Purification, characterization, and overexpression of an endo-1,4-β-mannanase from thermotolerant Bacillus sp. SWU60. World J. Microbiol. Biotechnol., 2017, 33(3), 53.
[http://dx.doi.org/10.1007/s11274-017-2224-7] [PMID: 28220352]
[19]
Gong, J.S.; Lu, Z.M.; Li, H.; Zhou, Z.M.; Shi, J.S.; Xu, Z.H. Metagenomic technology and genome mining: Emerging areas for exploring novel nitrilases. Appl. Microbiol. Biotechnol., 2013, 97(15), 6603-6611.
[http://dx.doi.org/10.1007/s00253-013-4932-8] [PMID: 23801047]
[20]
Itoh, T. Structures and functions of carbohydrate-active enzymes of chitinolytic bacteria Paenibacillus sp. str. FPU-7. Biosci. Biotechnol. Biochem., 2021, 85(6), 1314-1323.
[http://dx.doi.org/10.1093/bbb/zbab058] [PMID: 33792636]
[21]
Tang, C.D.; Shi, H.L.; Tang, Q.H.; Zhou, J.S.; Yao, L.G.; Jiao, Z.J.; Kan, Y.C. Genome mining and motif truncation of glycoside hydrolase family 5 endo-β-1,4-mannanase encoded by Aspergillus oryzae RIB40 for potential konjac flour hydrolysis or feed additive. Enzyme Microb. Technol., 2016, 93-94, 99-104.
[http://dx.doi.org/10.1016/j.enzmictec.2016.08.003] [PMID: 27702490]
[22]
Xie, H.; Poon, C.K.K.; Liu, H.; Wang, D.; Yang, J.; Han, Z. Molecular and biochemical characterizations of a new cold-active and mildly alkaline β-Mannanase from Verrucomicrobiae DG1235. Prep. Biochem. Biotechnol., 2021, 51(9), 881-891.
[http://dx.doi.org/10.1080/10826068.2020.1870235] [PMID: 33439094]
[23]
Almagro Armenteros, J.J.; Tsirigos, K.D.; Sønderby, C.K.; Petersen, T.N.; Winther, O.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol., 2019, 37(4), 420-423.
[http://dx.doi.org/10.1038/s41587-019-0036-z] [PMID: 30778233]
[24]
Williams, C.J.; Headd, J.J.; Moriarty, N.W.; Prisant, M.G.; Videau, L.L.; Deis, L.N.; Verma, V.; Keedy, D.A.; Hintze, B.J.; Chen, V.B.; Jain, S.; Lewis, S.M.; Arendall, W.B., III; Snoeyink, J.; Adams, P.D.; Lovell, S.C.; Richardson, J.S.; Richardson, D.C. MolProbity: More and better reference data for improved all-atom structure validation. Protein Sci., 2018, 27(1), 293-315.
[http://dx.doi.org/10.1002/pro.3330] [PMID: 29067766]
[25]
Studier, F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 2005, 41(1), 207-234.
[http://dx.doi.org/10.1016/j.pep.2005.01.016] [PMID: 15915565]
[26]
Hogg, D.; Pell, G.; Dupree, P.; Goubet, F.; Martín-Orúe, S.M.; Armand, S.; Gilbert, H.J. The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation. Biochem. J., 2003, 371(Pt 3), 1027-1043.
[http://dx.doi.org/10.1042/bj20021860] [PMID: 12523937]
[27]
Takasuka, T.E.; Acheson, J.F.; Bianchetti, C.M.; Prom, B.M.; Bergeman, L.F.; Book, A.J.; Currie, C.R.; Fox, B.G. Biochemical properties and atomic resolution structure of a proteolytically processed β-mannanase from cellulolytic Streptomyces sp. SirexAA-E. PLoS One, 2014, 9(4), e94166.
[http://dx.doi.org/10.1371/journal.pone.0094166] [PMID: 24710170]
[28]
Kumagai, Y.; Yamashita, K.; Tagami, T.; Uraji, M.; Wan, K.; Okuyama, M.; Yao, M.; Kimura, A.; Hatanaka, T. The loop structure of Actinomycete glycoside hydrolase family 5 mannanases governs substrate recognition. FEBS J., 2015, 282(20), 4001-4014.
[http://dx.doi.org/10.1111/febs.13401] [PMID: 26257335]
[29]
Santiago, M.; Ramírez-Sarmiento, C.A.; Zamora, R.A.; Parra, L.P. Discovery, molecular mechanisms, and industrial applications of cold-active enzymes. Front. Microbiol., 2016, 7, 1408.
[http://dx.doi.org/10.3389/fmicb.2016.01408] [PMID: 27667987]
[30]
Rao, T.E.; Imchen, M.; Kumavath, R. Marine enzymes: Production and applications for human health. Adv. Food Nutr. Res., 2017, 80, 149-163.
[http://dx.doi.org/10.1016/bs.afnr.2016.11.006] [PMID: 28215323]
[31]
Karbalaei, M.; Rezaee, S.A.; Farsiani, H. Pichia pastoris: A highly successful expression system for optimal synthesis of heterologous proteins. J. Cell. Physiol., 2020, 235(9), 5867-5881.
[http://dx.doi.org/10.1002/jcp.29583] [PMID: 32057111]
[32]
Aulitto, M.; Fusco, S.; Limauro, D.; Fiorentino, G.; Bartolucci, S.; Contursi, P. Galactomannan degradation by thermophilic enzymes: A hot topic for biotechnological applications. World J. Microbiol. Biotechnol., 2019, 35(2), 32.
[http://dx.doi.org/10.1007/s11274-019-2591-3] [PMID: 30701316]
[33]
Harnpicharnchai, P.; Pinngoen, W.; Teanngam, W.; Sornlake, W.; Sae-Tang, K.; Manitchotpisit, P.; Tanapongpipat, S. Production of high activity Aspergillus niger BCC4525 β-mannanase in Pichia pastoris and its application for mannooligosaccharides production from biomass hydrolysis. Biosci. Biotechnol. Biochem., 2016, 80(12), 2298-2305.
[http://dx.doi.org/10.1080/09168451.2016.1230003] [PMID: 27648762]
[34]
Shental-Bechor, D.; Levy, Y. Effect of glycosylation on protein folding: A close look at thermodynamic stabilization. Proc. Natl. Acad. Sci. USA, 2008, 105(24), 8256-8261.
[http://dx.doi.org/10.1073/pnas.0801340105] [PMID: 18550810]
[35]
Zhou, C.; Xue, Y.; Ma, Y. Characterization and high-efficiency secreted expression in Bacillus subtilis of a thermo-alkaline β-mannanase from an alkaliphilic Bacillus clausii strain S10. Microb. Cell Fact., 2018, 17(1), 124.
[http://dx.doi.org/10.1186/s12934-018-0973-0] [PMID: 30098601]
[36]
Do, B.C.; Dang, T.T.; Berrin, J.G.; Haltrich, D.; To, K.A.; Sigoillot, J.C.; Yamabhai, M. Cloning, expression in Pichia pastoris, and characterization of a thermostable GH5 mannan endo-1,4-beta-mannosidase from Aspergillus niger BK01. Microb. Cell Fact., 2009, 8(1), 59.
[http://dx.doi.org/10.1186/1475-2859-8-59] [PMID: 19912637]

Rights & Permissions Print Cite
Article Metrics
3
© 2024 Bentham Science Publishers | Privacy Policy