Heteroxylan hydrolysis by a recombinant cellulase-free GH10 xylanase from the alkaliphilic bacterium Halalkalibacterium halodurans C-125.
Substrate Specificity
Hydrolysis
Xylans
/ metabolism
Endo-1,4-beta Xylanases
/ metabolism
Recombinant Proteins
/ metabolism
Escherichia coli
/ genetics
Hydrogen-Ion Concentration
Cloning, Molecular
Bacterial Proteins
/ genetics
Glucuronates
/ metabolism
Enzyme Stability
Kinetics
Molecular Weight
Oligosaccharides
/ metabolism
Disaccharides
Halalkalibacterium halodurans C-125
Active xylooligosaccharides
Alkaliphilicity
Cellulase-free
GH10 xylanase
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
16 May 2024
16 May 2024
Historique:
received:
03
03
2024
accepted:
25
04
2024
revised:
13
04
2024
medline:
16
5
2024
pubmed:
16
5
2024
entrez:
16
5
2024
Statut:
epublish
Résumé
The search for affordable enzymes with exceptional characteristics is fundamental to overcoming industrial and environmental constraints. In this study, a recombinant GH10 xylanase (Xyn10-HB) from the extremely alkaliphilic bacterium Halalkalibacterium halodurans C-125 cultivated at pH 10 was cloned and expressed in E. coli BL21(DE3). Removal of the signal peptide improved the expression, and an overall activity of 8 U/mL was obtained in the cell-free supernatant. The molecular weight of purified Xyn10-HB was estimated to be 42.6 kDa by SDS-PAGE. The enzyme was active across a wide pH range (5-10) with optimal activity recorded at pH 8.5 and 60 °C. It also presented good stability with a half-life of 3 h under these conditions. Substrate specificity studies showed that Xyn10-HB is a cellulase-free enzyme that conventionally hydrolyse birchwood and oat spelts xylans (Apparent K
Identifiants
pubmed: 38753095
doi: 10.1007/s00203-024-03982-w
pii: 10.1007/s00203-024-03982-w
doi:
Substances chimiques
xylobiose
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
261Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Aachary AA, Prapulla SG (2009) Value addition to corncob: production and characterization of xylooligosaccharides from alkali pretreated lignin-saccharide complex using Aspergillus oryzae MTCC 5154. Bioresour Technol 100:991–995. https://doi.org/10.1016/j.biortech.2008.06.050
doi: 10.1016/j.biortech.2008.06.050
pubmed: 18703333
Bai W, Xue Y, Zhou C, Ma Y (2012) Cloning, expression and characterization of a novel salt-tolerant xylanase from Bacillus sp. SN5. Biotechnol Lett 34:2093–2099. https://doi.org/10.1007/s10529-012-1011-7
doi: 10.1007/s10529-012-1011-7
pubmed: 22864505
Bhardwaj A, Bharadwaj A, Leelavathi S et al (2008) The critical role of partially exposed N-terminal valine residue in stabilizing GH10 xylanase from Bacillus sp. NG-27 under poly-extreme conditions. PLoS ONE 3:e3063. https://doi.org/10.1371/journal.pone.0003063
doi: 10.1371/journal.pone.0003063
pubmed: 18725971
Bhardwaj N, Kumar B, Verma P (2019) A detailed overview of xylanases: an emerging biomolecule for current and future prospective. Bioresour Bioprocess 6:40. https://doi.org/10.1186/s40643-019-0276-2
doi: 10.1186/s40643-019-0276-2
Biely P, Vršanská M, Tenkanen M, Kluepfel D (1997) Endo-β-1,4-xylanase families: differences in catalytic properties. J Biotechnol 57:151–166. https://doi.org/10.1016/S0168-1656(97)00096-5
doi: 10.1016/S0168-1656(97)00096-5
pubmed: 9335171
Chakdar H, Kumar M, Pandiyan K et al (2016) Bacterial xylanases: biology to biotechnology. 3 Biotech 6:150. https://doi.org/10.1007/s13205-016-0457-z
doi: 10.1007/s13205-016-0457-z
pubmed: 28330222
pmcid: 4929084
Chang P, Tsai W-S, Tsai C-L, Tseng M-J (2004) Cloning and characterization of two thermostable xylanases from an alkaliphilic Bacillus firmus. Biochem Biophys Res Commun 319:1017–1025. https://doi.org/10.1016/j.bbrc.2004.05.078
doi: 10.1016/j.bbrc.2004.05.078
pubmed: 15184083
Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23. https://doi.org/10.1016/j.femsre.2004.06.005
doi: 10.1016/j.femsre.2004.06.005
pubmed: 15652973
de Menezes CR, Silva ÍS, Pavarina ÉC et al (2009) Production of xylooligosaccharides from enzymatic hydrolysis of xylan by the white-rot fungi Pleurotus. Int Biodeterior Biodegrad 63:673–678. https://doi.org/10.1016/j.ibiod.2009.02.008
doi: 10.1016/j.ibiod.2009.02.008
El-Gendi H, Badawy AS, Bakhiet EK, Rawway M, Ali SG (2023) Valorization of lignocellulosic wastes for sustainable xylanae production from locally isolated Bacillus subtilis exploited for xylooligosaccharides production with potential antimicrobial activity. Arch Microbiol 205:315. https://doi.org/10.1007/s00203-023-03645-2
doi: 10.1007/s00203-023-03645-2
pubmed: 37605001
pmcid: 10442310
Faulds CB, Mandalari G, Lo Curto RB et al (2006) Synergy between xylanases from glycoside hydrolase family 10 and family 11 and a feruloyl esterase in the release of phenolic acids from cereal arabinoxylan. Appl Microbiol Biotechnol 71:622–629. https://doi.org/10.1007/s00253-005-0184-6
doi: 10.1007/s00253-005-0184-6
pubmed: 16292533
Fuso A, Dejonghe W, Cauwenberghs L, Rosso G, Rosso F, Manera I, Caligiani A (2023) DPPH radical scavenging activity of xylo-oligosaccharides mixtures of controlled composition: a step forward in understanding structure–activity relationship. J Funct Foods 101:105417. https://doi.org/10.1016/j.jff.2023.105417
doi: 10.1016/j.jff.2023.105417
Glekas PD, Kalantzi S, Dalios A et al (2022) Biochemical and thermodynamic studies on a novel thermotolerant GH10 xylanase from Bacillus safensis. Biomolecules 12:790. https://doi.org/10.3390/biom12060790
doi: 10.3390/biom12060790
pubmed: 35740915
pmcid: 9221164
Gupta N, Reddy VS, Maiti S, Ghosh A (2000) Cloning, expression, and sequence analysis of the gene encoding the alkali-stable, thermostable endoxylanase from alkalophilic, mesophilic Bacillus sp. strain NG-27. Appl Environ Microbiol 66:2631–2635
doi: 10.1128/AEM.66.6.2631-2635.2000
pubmed: 10831448
pmcid: 110591
Henrissat B, Callebaut I, Fabrega S et al (1995) Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proc Natl Acad Sci USA 92:7090–7094
doi: 10.1073/pnas.92.15.7090
pubmed: 7624375
pmcid: 41477
Honda H, Kudo T, Horikoshi K (1985) Molecular cloning and expression of the xylanase gene of alkalophilic Bacillus sp. strain C-125 in Escherichia coli. J Bacteriol 161:784–785
doi: 10.1128/jb.161.2.784-785.1985
pubmed: 3881413
pmcid: 214955
Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol Rev 63:735–750. https://doi.org/10.1128/MMBR.63.4.735-750.1999
doi: 10.1128/MMBR.63.4.735-750.1999
pubmed: 10585964
pmcid: 98975
Hu J, Arantes V, Saddler JN (2011) The enhancement of enzymatic hydrolysis of lignocellulosic substrates by the addition of accessory enzymes such as xylanase: is it an additive or synergistic effect? Biotechnol Biofuels 4:36. https://doi.org/10.1186/1754-6834-4-36
doi: 10.1186/1754-6834-4-36
pubmed: 21974832
pmcid: 3198685
Jain I, Kumar V, Satyanarayana T (2015) Xylooligosaccharides: an economical prebiotic from agroresidues and their health benefits. Indian J Exp Biol 53:131–142
pubmed: 25872243
Jiang Z, Lierop B, Nolin A, Berry R (2003) A new insight into the bleachability of kraft pulps. J Pulp Paper Sci 29(2):54–58
Jmel MA, Anders N, Ben Yahmed N et al (2020) Efficient enzymatic saccharification of macroalgal biomass using a specific thermostable GH 12 endoglucanase from Aspergillus terreus JL1. World J Microbiol Biotechnol 36:5. https://doi.org/10.1007/s11274-019-2779-6
doi: 10.1007/s11274-019-2779-6
Jomrit J, Suhardi S, Summpunn P (2023) Effects of signal peptide and chaperone co-expression on heterologous protein production in Escherichia coli. Molecules 28(14):5594. https://doi.org/10.3390/molecules28145594
doi: 10.3390/molecules28145594
pubmed: 37513466
pmcid: 10384211
Joshi N, Sharma M, Singh SP (2020) Characterization of a novel xylanase from an extreme temperature hot spring metagenome for xylooligosaccharide production. Appl Microbiol Biotechnol 104:4889–4901. https://doi.org/10.1007/s00253-020-10562-7
doi: 10.1007/s00253-020-10562-7
pubmed: 32249395
Jun H, Bing Y, Keying Z, Daiwen C (2009) Functional characterization of a recombinant thermostable xylanase from Pichia pastoris: a hybrid enzyme being suitable for xylooligosaccharides production. Biochem Eng J 48:87–92. https://doi.org/10.1016/j.bej.2009.08.010
doi: 10.1016/j.bej.2009.08.010
Kumar V, Satyanarayana T (2013) Biochemical and thermodynamic characteristics of thermo-alkali-stable xylanase from a novel polyextremophilic Bacillus halodurans TSEV1. Extrem Life Extreme Cond 17:797–808. https://doi.org/10.1007/s00792-013-0565-1
doi: 10.1007/s00792-013-0565-1
Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
doi: 10.1038/227680a0
pubmed: 5432063
Lai Z, Zhou C, Ma X et al (2021) Enzymatic characterization of a novel thermostable and alkaline tolerant GH10 xylanase and activity improvement by multiple rational mutagenesis strategies. Int J Biol Macromol 170:164–177. https://doi.org/10.1016/j.ijbiomac.2020.12.137
doi: 10.1016/j.ijbiomac.2020.12.137
pubmed: 33352153
Li H, Xiong L, Chen X et al (2019) Enhanced enzymatic hydrolysis of wheat straw via a combination of alkaline hydrogen peroxide and lithium chloride/N,N-dimethylacetamide pretreatment. Ind Crops Prod 137:332–338. https://doi.org/10.1016/j.indcrop.2019.05.027
doi: 10.1016/j.indcrop.2019.05.027
Li Y, Zhang X, Lu C et al (2022) Identification and characterization of a novel endo-β-1,4-Xylanase from Streptomyces sp. T7 and its application in xylo-oligosaccharide production. Molecules 27:2516. https://doi.org/10.3390/molecules27082516
doi: 10.3390/molecules27082516
pubmed: 35458713
pmcid: 9032680
Lin X, Han S, Zhang N et al (2013) Bleach boosting effect of xylanase A from Bacillus halodurans C-125 in ECF bleaching of wheat straw pulp. Enzyme Microb Technol 52:91–98. https://doi.org/10.1016/j.enzmictec.2012.10.011
doi: 10.1016/j.enzmictec.2012.10.011
pubmed: 23273277
Mahmood MS, Rasul F, Saleem M et al (2019) Characterization of recombinant endo-1,4-β-xylanase of Bacillus halodurans C-125 and rational identification of hot spot amino acid residues responsible for enhancing thermostability by an in-silico approach. Mol Biol Rep 46:3651–3662. https://doi.org/10.1007/s11033-019-04751-5
doi: 10.1007/s11033-019-04751-5
pubmed: 31079316
Mamo G, Delgado O, Martinez A et al (2006a) Cloning, sequence analysis, and expression of a gene encoding an endoxylanase from Bacillus halodurans S7. Mol Biotechnol 33:149–159. https://doi.org/10.1385/MB:33:2:149
doi: 10.1385/MB:33:2:149
pubmed: 16757802
Mamo G, Hatti-Kaul R, Mattiasson B (2006b) A thermostable alkaline active endo-β-1-4-xylanase from Bacillus halodurans S7: purification and characterization. Enzyme Microb Technol 39:1492–1498. https://doi.org/10.1016/j.enzmictec.2006.03.040
doi: 10.1016/j.enzmictec.2006.03.040
Mamo G, Thunnissen M, Hatti-Kaul R, Mattiasson B (2009) An alkaline active xylanase: insights into mechanisms of high pH catalytic adaptation. Biochimie 91:1187–1196. https://doi.org/10.1016/j.biochi.2009.06.017
doi: 10.1016/j.biochi.2009.06.017
pubmed: 19567261
Manikandan K, Bhardwaj A, Gupta N et al (2006) Crystal structures of native and xylosaccharide-bound alkali thermostable xylanase from an alkalophilic Bacillus sp. NG-27: structural insights into alkalophilicity and implications for adaptation to polyextreme conditions. Protein Sci Publ Protein Soc 15:1951–1960. https://doi.org/10.1110/ps.062220206
doi: 10.1110/ps.062220206
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
doi: 10.1021/ac60147a030
Motta F, C P Andrade C, Santana MH, (2013) A review of xylanase production by the fermentation of xylan: classification, characterization and applications. Sustain Degrad Lignocellul Biomass Tech Appl Commer. https://doi.org/10.5772/53544
doi: 10.5772/53544
Mukherjee A, Sarkar S, Gupta S, Banerjee S, Senapati S, Chakrabarty R, Gachhui R (2019) DMSO strengthens chitin deacetylase-chitin interaction: physicochemical, kinetic, structural and catalytic insights. Carbohydr Polym 223:115032. https://doi.org/10.1016/j.carbpol.2019.115032
doi: 10.1016/j.carbpol.2019.115032
pubmed: 31426990
Nakamura S, Nakai R, Wakabayashi K et al (1994) Thermophilic alkaline xylanase from newly isolated alkaliphilic and thermophilic Bacillus sp. strain TAR-1. Biosci Biotechnol Biochem 58:78–81. https://doi.org/10.1271/bbb.58.78
doi: 10.1271/bbb.58.78
pubmed: 27315708
Nakatani K, Katano Y, Kojima K et al (2018) Increase in the thermostability of Bacillus sp. strain TAR-1 xylanase using a site saturation mutagenesis library. Biosci Biotechnol Biochem 82:1715–1723. https://doi.org/10.1080/09168451.2018.1495550
doi: 10.1080/09168451.2018.1495550
pubmed: 30001680
Rashid R, Sohail M (2021) Xylanolytic Bacillus species for xylooligosaccharides production: a critical review. Bioresour Bioprocess 8:16. https://doi.org/10.1186/s40643-021-00369-3
doi: 10.1186/s40643-021-00369-3
pubmed: 38650226
pmcid: 10991489
Rodríguez-Sanz A, Fuciños C, Torrado AM, Rúa ML (2022) Extraction of the wheat straw hemicellulose fraction assisted by commercial endo-xylanase Role of the accessory enzyme activities. Ind Crops Prod 179:114655. https://doi.org/10.1016/j.indcrop.2022.114655
doi: 10.1016/j.indcrop.2022.114655
Selvarajan E, Veena R (2017) Recent advances and future. Perspect Thermostab Xylanase. https://doi.org/10.13005/BBRA
doi: 10.13005/BBRA
Sharma PK (2017) Xylanases current and future perspectives: a review. New Biol Rep 6:12–22
Shrestha S, Khatiwada R, Kognou AL, Chio C, Qin W (2023) A comparative study of Cellulomonas sp. and Bacillus sp. in utilizing lignocellulosic biomass as feedstocks for enzyme production. Arch Microbiol 205:130. https://doi.org/10.1007/s00203-023-03470-7
doi: 10.1007/s00203-023-03470-7
pubmed: 36947219
Siwach R, Sharma S, Ali Khan A, Kumar A, Agrawal S (2024) Optimization of xylanase production by Bacillus sp MCC2212 under solid-state fermentation using response surface methodology. Biocatal Agric Biotechnol 57:103085. https://doi.org/10.1016/j.bcab.2024.103085
doi: 10.1016/j.bcab.2024.103085
Smaali I, Rémond C, O’Donohue MJ (2006) Expression in Escherichia coli and characterization of beta-xylosidases GH39 and GH-43 from Bacillus halodurans C-125. Appl Microbiol Biotechnol 73:582–590. https://doi.org/10.1007/s00253-006-0512-5
doi: 10.1007/s00253-006-0512-5
pubmed: 16896606
Smaali I, Maugard T, Limam F et al (2007) Efficient synthesis of gluco-oligosaccharides and alkyl-glucosides by transglycosylation activity of β-glucosidase from Sclerotinia sclerotiorum. World J Microbiol Biotechnol 23:145–149. https://doi.org/10.1007/s11274-006-9185-6
doi: 10.1007/s11274-006-9185-6
Smaali I, Rémond C, Skhiri Y, O’Donohue MJ (2009) Biocatalytic conversion of wheat bran hydrolysate using an immobilized GH43 β-xylosidase. Bioresour Technol 100:338–344. https://doi.org/10.1016/j.biortech.2008.06.041
doi: 10.1016/j.biortech.2008.06.041
pubmed: 18674896
Takami H, Horikoshi K (2000) Analysis of the genome of an alkaliphilic Bacillus strain from an industrial point of view. Extrem Life Extreme Cond 4:99–108. https://doi.org/10.1007/s007920050143
doi: 10.1007/s007920050143
Takami H, Takaki Y, Nakasone K et al (1999) Genetic analysis of the chromosome of alkaliphilic Bacillus halodurans C-125. Extrem Life Extreme Cond 3:227–233. https://doi.org/10.1007/s007920050120
doi: 10.1007/s007920050120
Takami H, Nakasone K, Takaki Y 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
doi: 10.1093/nar/28.21.4317
pubmed: 11058132
pmcid: 113120
Tung KK, Nordin JH (1969) Determination of the action patterns of glycanases. Anal Biochem 29:84–90. https://doi.org/10.1016/0003-2697(69)90010-4
doi: 10.1016/0003-2697(69)90010-4
pubmed: 5813843
Verma D (2021) Extremophilic prokaryotic endoxylanases: diversity, applicability, and molecular insights. Front Microbiol 12:728475. https://doi.org/10.3389/fmicb.2021.728475
doi: 10.3389/fmicb.2021.728475
pubmed: 34566933
pmcid: 8458939
Verma D, Satyanarayana T (2012) Cloning, expression and applicability of thermo-alkali-stable xylanase of Geobacillus thermoleovorans in generating xylooligosaccharides from agro-residues. Bioresour Technol 107:333–338. https://doi.org/10.1016/j.biortech.2011.12.055
doi: 10.1016/j.biortech.2011.12.055
pubmed: 22212694
Wang K, Cao R, Wang M et al (2019) A novel thermostable GH10 xylanase with activities on a wide variety of cellulosic substrates from a xylanolytic Bacillus strain exhibiting significant synergy with commercial Celluclast 1.5 L in pretreated corn stover hydrolysis. Biotechnol Biofuels 12:48. https://doi.org/10.1186/s13068-019-1389-8
doi: 10.1186/s13068-019-1389-8
pubmed: 30899328
pmcid: 6408826
Wei H, Chen X, Shekiro J et al (2018) Kinetic modelling and experimental studies for the effects of Fe
doi: 10.3390/catal8010039
Wiater A, Waśko A, Adamczyk P et al (2020) Prebiotic potential of oligosaccharides obtained by acid hydrolysis of α-(1→3)-glucan from Laetiporus sulphureus: a pilot study. Molecules 25:5542. https://doi.org/10.3390/molecules25235542
doi: 10.3390/molecules25235542
pubmed: 33255915
pmcid: 7728339
Yang J, Yan R, Roy A et al (2015) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12:7–8. https://doi.org/10.1038/nmeth.3213
doi: 10.1038/nmeth.3213
pubmed: 25549265
pmcid: 4428668
Yegin S (2022) Microbial xylanases in xylooligosaccharide production from lignocellulosic feedstocks. Biomass Convers Biorefin. https://doi.org/10.1007/s13399-022-03190-w
doi: 10.1007/s13399-022-03190-w
Zhang G, Mao L, Zhao Y et al (2010) Characterization of a thermostable xylanase from an alkaliphilic Bacillus sp. Biotechnol Lett 32:1915–1920. https://doi.org/10.1007/s10529-010-0372-z
doi: 10.1007/s10529-010-0372-z
pubmed: 20730475
Zhou J, Dong Y, Tang X et al (2012) Molecular and biochemical characterization of a novel intracellular low-temperature-active xylanase. J Microbiol Biotechnol 22:501–509. https://doi.org/10.4014/jmb.1108.08006
doi: 10.4014/jmb.1108.08006
pubmed: 22534297