Abstract
Thermoalkaliphilic GH11 xylanases are largely favored for paper pulp biobleaching process. The present work aimed to comparatively investigate the molecular phylogeny, amino acid sequences, molecular structure, and enzyme–substrate interaction of six thermoalkaliphilic GH11 xylanases from different bacterial species (Oxalobacteraceae bacterium xylanase = ObXyl, Sphingomonas sp. xylanase = SsXyl, Hymenobacter sp. xylanase = HsXyl, Amycolatopsis vastitatis xylanase = AvXyl, Lentzea deserti xylanase = LdXyl, Streptomyces rubellomurinus xylanase = SrXyl). For this purpose, six bacterial thermoalkaliphilic GH11 xylanase sequences derived from unreviewed protein entries of UniProt/TrEMBL database were analyzed for their phylogenetic relationships and sequence similarities. Also, 3D predicted structures of the enzymes were built and computationally validated by different bioinformatics tools. The enzyme–substrate interactions were investigated by molecular docking analysis using various substrates. Phylogenetic analysis showed that six enzymes were grouped into two different clusters: the first cluster included ObXyl, SsXyl, and HsXyl, whereas the second cluster had AvXyl, LdXyl, and SrXyl. Multiple sequence alignment showed that the second cluster xylanases possessed longer N-terminal regions indicating higher thermostability, compared to the first cluster xylanases. The structural analyses showed that six predicted structures were largely conserved. Molecular docking results indicated that binding efficiency to xylotriose, xylotetraose, and xylopentaose was higher in second cluster enzymes than that in first cluster enzymes, exhibiting mostly above -8.0 kCal/mol of binding energy. Arginine in B8 β-strand was commonly involved in substrate interactions in all the second cluster xylanases, different from the first cluster ones. Thus, the present work predicted that the thermoalkaliphilic xylanases in the second cluster might be greater potential candidates for the paper pulp bleaching process.
Similar content being viewed by others
Abbreviations
- CAZy:
-
Carbohydrate Active Enzymes
- GH:
-
Glycoside Hydrolase
- WGS:
-
Whole-Genome Shotgun WGS
- pI:
-
Isoelectric Point
- Tm :
-
Melting Temperature
- NCR:
-
Negatively Charged Residues
- PCR:
-
Positively Charged Residues
- ML:
-
Maximum Likelihood
- JTT:
-
Jones-Taylor-Thornton
- LGA:
-
Lamarckian Genetic Algorithm
- SDF:
-
Spatial Data File
- PDB:
-
Protein Data Bank
- ObXyl:
-
Oxalobacteraceae Bacterium xylanase
- SsXyl:
-
Sphingomonas sp. Xylanase
- HsXyl:
-
Hymenobacter sp. Xylanase
- AvXyl:
-
Amycolatopsis vastitatis Xylanase
- LdXyl:
-
Lentzea deserti Xylanase
- SrXyl:
-
Streptomyces rubellomurinus Xylanase
- Tx-xyl:
-
Xylanase from Thermobacillus xylanilyticus
- GMQE:
-
Global Model Quality Estimate
- UniProt:
-
The Universal Protein Knowledgebase
- X2 :
-
Xylobiose
- X3 :
-
Xylotriose
- X4 :
-
Xylotetraose
- X5 :
-
Xylopentaose
References
Adamek M, Alanjary M, Sales-Ortells H, Goodfellow M, Bull AT, Winkler A, Wibberg D, Kalinowski J, Ziemert N (2018) Comparative genomics reveals phylogenetic distribution patterns of secondary metabolites in Amycolatopsis species. BMC Genom 19:426. https://doi.org/10.1186/s12864-018-4809-4
Algan M, Sürmeli Y, Şanlı-Mohamed G (2021) A novel thermostable xylanase from Geobacillus vulcani GS90: Production, biochemical characterization, and its comparative application in fruit juice enrichment. J Food Biochem 45(5):e13716. https://doi.org/10.1111/JFBC.13716
Bajpai P (1999) Application of enzymes in the pulp and paper industry. Biotechnol Prog 15(2):147–157. https://doi.org/10.1021/BP990013K
Basu M, Kumar V, Shukla P (2018) Recombinant approaches for microbial xylanases: recent advances and perspectives. Curr Protein Pept Sci 19:87–99. https://doi.org/10.2174/1389203718666161122110200
Bauer S, Vasu P, Persson S, Mort AJ, Somerville CR (2006) Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. PNAS 103(30):11417–11422. https://doi.org/10.1073/PNAS.0604632103
Beg QK, Kapoor M, Mahajan L, Hoondal GS (2001) Microbial xylanases and their industrial applications: A review. Appl Microbiol Biotechnol 56(3–4):326–338. https://doi.org/10.1007/s002530100704
Berrin JG, Ajandouz EH, Georis J, Arnaut F, Juge N (2007) Substrate and product hydrolysis specificity in family 11 glycoside hydrolases: an analysis of Penicillium funiculosum and Penicillium griseofulvum xylanases. Appl Microbiol Biotechnol 74(5):1001–1010. https://doi.org/10.1007/S00253-006-0764-0
Boonyapakron K, Jaruwat A, Liwnaree B, Nimchua T, Champreda V, Chitnumsub P (2017) Structure-based protein engineering for thermostable and alkaliphilic enhancement of endo-β-1,4-xylanase for applications in pulp bleaching. J Biotechnol 259:95–102. https://doi.org/10.1016/J.JBIOTEC.2017.07.035
Bowie JU, Lüthy R, Eisenberg D (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253(5016):164–170. https://doi.org/10.1126/SCIENCE.1853201
Briganti L, Capetti C, Pellegrini VOA, Ghio S, Campos E, Nascimento AS, Polikarpov I (2021) Structural and molecular dynamics investigations of ligand stabilization via secondary binding site interactions in Paenibacillus xylanivorans GH11 xylanase. Comput Struct Biotechnol J 19:1557–1566. https://doi.org/10.1016/j.csbj.2021.03.002
Chadha BS, Kaur B, Basotra N, Tsang A, Pandey A (2019) Thermostable xylanases from thermophilic fungi and bacteria: Current perspective. Bioresour Technol 277:195–203. https://doi.org/10.1016/J.BIORTECH.2019.01.044
Chakdar H, Kumar M, Pandiyan K, Singh A, Nanjappan K, Kashyap PL, Srivastava AK (2016) Bacterial xylanases: biology to biotechnology. 3 Biotech 6(2). https://doi.org/10.1007/S13205-016-0457-Z
Cheng YS, Chen CC, Huang CH, Ko TP, Luo W, Huang JW, Liu JR, Guo RT (2014) Structural analysis of a glycoside hydrolase family 11 xylanase from Neocallimastix patriciarum : Insights into the molecular basis of a thermophilic enzyme. J Biol Chem 289:11020–11028. https://doi.org/10.1074/jbc.M114.550905
Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29(1):3–23. https://doi.org/10.1016/j.femsre.2004.06.005
Crombie AT, Larke-Mejia NL, Emery H, Dawson R, Pratscher J, Murphy GP, McGenity TJ, Murrell JC (2018) Poplar phyllosphere harbors disparate isoprene-degrading bacteria. PNAS 115(51):13081–13086. https://doi.org/10.1073/pnas.1812668115
Debeire-Gosselin M, Loonis M, Samain E, Debeire P (1992) Purification and properties of a 22 kDa endoxylanase excreted by a new strain of thermophilic Bacillus. In: Visser J, Beldman G, van Someren MA Kusters-, Voragen AGJ, (eds). Xylans and xylanases. Amsterdam, The Netherlands: Elsevier Science Publishers B.V., pp. 463–466
Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B, Terrapon N (2022) The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 50(D1):D571–D577. https://doi.org/10.1093/nar/gkab1045
Gagné D, Narayanan C, Nguyen-Thi N, Roux LD, Bernard DN, Brunzelle JS, Couture JF, Agarwal PK, Doucet N (2016) Ligand Binding Enhances Millisecond Conformational Exchange in Xylanase B2 from Streptomyces lividans. Biochemistry 55(30):4184–4196. https://doi.org/10.1021/ACS.BIOCHEM.6B00130/SUPPL_FILE/BI6B00130_SI_001.PDF
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein Identification and Analysis Tools on the ExPASy Server. In: Walker JM (eds) The Proteomics protocols handbook, Springer Protocols Handbooks, Humana Press. https://doi.org/10.1385/1-59259-890-0:571
Hakulinen N, Turunen O, Jänis J, Leisola M, Rouvinen J (2003) Three-dimensional structures of thermophilic β-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa. FEBS J 270(7):1399–1412. https://doi.org/10.1046/J.1432-1033.2003.03496.X
Han N, Miao H, Ding J, Li J, Mu Y, Zhou J, Huang Z (2017) Improving the thermostability of a fungal GH11 xylanase via site-directed mutagenesis guided by sequence and structural analysis. Biotechnol Biofuels 10:133. https://doi.org/10.1186/s13068-017-0824-y
Harris GW, Jenkins JA, Connerton I, Cummings N, Lo LL, Scott M, Hazlewood GP, Laurie JI, Gilbert HJ, Pickersgill RW (1994) Structure of the catalytic core of the family F xylanase from Pseudomonas fluorescens and identification of the xylopentaose-binding sites. Structure 2(11):1107–1116. https://doi.org/10.1016/S0969-2126(94)00112-X
Heinig M, Frishman D (2004) STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Res 32:W500. https://doi.org/10.1093/NAR/GKH429
Jommuengbout P, Pinitglang S, Kyu KL, Ratanakhanokchai K (2009) Substrate-binding site of family 11 xylanase from Bacillus firmus K-1 by molecular docking. Biosci Biotechnol Biochem 73(4):833–839. https://doi.org/10.1271/bbb.80731
Khandeparkar RDS, Bhosle NB (2006) Isolation, purification and characterization of the xylanase produced by Arthrobacter sp. MTCC 5214 when grown in solid-state fermentation. Enzyme Microb Technol 39(4):732–742. https://doi.org/10.1016/J.ENZMICTEC.2005.12.008
Ku T, Lu P, Chan C, Wang T, Lai S, Lyu P, Hsiao N (2009) Predicting melting temperature directly from protein sequences. Comput Biol Chem 33(6):445–450. https://doi.org/10.1016/J.COMPBIOLCHEM.2009.10.002
Kumar A, Gautam A, Dutt D, Yadav M, Sehrawat N, Kumar P (2017) Applications of microbial technology in pulp and paper industry. ln: Kumar A, Dutt D, Yadav M (eds), Microbiology and biotechnology for a sustainable environment, 1st edn. Nova Science Publishers: New York, pp 185–206
Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA (1999) An Arabidopsis gene encoding a chloroplast-targeted beta-amylase. Plant J 20(5):519–527. https://doi.org/10.1046/J.1365-313X.1999.00625.X
Laskowski RA, Rullmann JAC, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8(4):477–486. https://doi.org/10.1007/BF00228148
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey ARN, Potter SC, Finn RD, Lopez R (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47(W1):W636–W641. https://doi.org/10.1093/NAR/GKZ268
Mamo G, Thunnissen M, Hatti-Kaul R, Mattiasson B (2009) An alkaline active xylanase: Insights into mechanisms of high pH catalytic adaptation. Biochimie 91(9):1187–1196. https://doi.org/10.1016/J.BIOCHI.2009.06.017
Mirdita M, Von Den Driesch L, Galiez C, Martin MJ, Soding J, Steinegger M (2017) Uniclust databases of clustered and deeply annotated protein sequences and alignments. Nucleic Acids Res 45(D1):D170–D176. https://doi.org/10.1093/NAR/GKW1081
Motta FL, Andrade CCP, Santana MHA (2013) A Review of Xylanase Production by the Fermentation of Xylan: Classification, Characterization and Applications. ln Chandel AK, Da Silva SS (eds) Sustainable degradation of lignocellulosic biomass - techniques, applications and commercialization, IntechOpen, London. https://doi.org/10.5772/53544
Nordberg Karlsson E, Schmitz E, Linares-Pastén JA, Adlercreutz P (2018) Endo-xylanases as tools for production of substituted xylooligosaccharides with prebiotic properties. Appl Microbiol Biotechnol 102(21):9081–9088. https://doi.org/10.1007/S00253-018-9343-4
Paës G, Berrin JG, Beaugrand J (2012) GH11 xylanases: Structure/function/properties relationships and applications. Biotechnol Adv 30(3):564–592. https://doi.org/10.1016/J.BIOTECHADV.2011.10.003
Pollet A, Beliën T, Fierens K, Delcour JA, Courtin CM (2009) Fusarium graminearum xylanases show different functional stabilities, substrate specificities and inhibition sensitivities. Enzyme Microb Technol 44(4):189–195. https://doi.org/10.1016/J.ENZMICTEC.2008.12.005
Raj A, Kumar S, Singh SK (2013) A highly thermostable xylanase from Stenotrophomonas maltophilia: Purification and partial characterization. Enzyme Res 2013:429305. https://doi.org/10.1155/2013/429305
Sabini E, Sulzenbacher G, Dauter M, Dauter Z, Jørgensen PL, Schülein M, Dupont C, Davies GJ, Wilson KS (1999) Catalysis and specificity in enzymatic glycoside hydrolysis: a 2,5B conformation for the glycosyl-enzyme intermediate revealed by the structure of the Bacillus agaradhaerens family 11 xylanase. Chem Biol 6(7):483–492. https://doi.org/10.1016/S1074-5521(99)80066-0
Sánchez ÓJ, Cardona CA (2008) Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour Technol 99(13):5270–5295. https://doi.org/10.1016/J.BIORTECH.2007.11.013
Steinegger M, Meier M, Mirdita M, Vöhringer H, Haunsberger SJ, Söding J (2019) HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinform 20(1):1–15. https://doi.org/10.1186/S12859-019-3019-7/FIGURES/7
Studer G, Studer G, Rempfer C, Rempfer C, Waterhouse AM, Waterhouse AM, Gumienny R, Gumienny R, Haas J, Haas J, Schwede T, Schwede T (2020) QMEANDisCo—distance constraints applied on model quality estimation. Bioinformatics 36(8):2647–2647. https://doi.org/10.1093/BIOINFORMATICS/BTAA058
Studer G, Tauriello G, Bienert S, Biasini M, Johner N, Schwede T (2021) ProMod3-A versatile homology modelling toolbox. PLoS Comput Biol 17(1). https://doi.org/10.1371/JOURNAL.PCBI.1008667
Subramaniyan S, Prema P (2002) Biotechnology of microbial xylanases: enzymology, molecular biology, and application. Crit Rev Biotechnol 22(1):33–64. https://doi.org/10.1080/07388550290789450
Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38(7):3022–3027. https://doi.org/10.1093/MOLBEV/MSAB120
The UniProt Consortium (2021) UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res 49(D1):D480–D489. https://doi.org/10.1093/nar/gkaa1100
Törrönen A, Harkki A, Rouvinen J (1994) Three-dimensional structure of endo-1,4-beta-xylanase II from Trichoderma reesei: two conformational states in the active site. EMBO J 13(11):2493. https://doi.org/10.1002/j.1460-2075.1994.tb06536.x
Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading. J Comput Chem 31(2):455. https://doi.org/10.1002/JCC.21334
Valenzuela SV, Diaz P, Pastor FIJ (2014) Xyn11E from Paenibacillus barcinonensis BP-23: a LppX-chaperone-dependent xylanase with potential for upgrading paper pulps. Appl Microbiol Biotechnol 98(13):5949–5957. https://doi.org/10.1007/S00253-014-5565-2
Vardakou M, Dumon C, Murray JW, Christakopoulos P, Weiner DP, Juge N, Lewis RJ, Gilbert HJ, Flint JE (2008) Understanding the Structural Basis for Substrate and Inhibitor Recognition in Eukaryotic GH11 Xylanases. J Mol Biol 375(5):1293–1305. https://doi.org/10.1016/J.JMB.2007.11.007
Wakarchuk WW, Robert L, Campbell RL, Sung WL, Davoodi J, Yaguchi M (1994) Mutational and crystallographic analyses of the active site residues of the Bacillus circulans xylanase. Protein Sci 3:467–475. https://doi.org/10.1002/pro.5560030312
Wang S, Li W, Liu S, Xu J (2016) RaptorX-Property: a web server for protein structure property prediction. Nucleic Acids Res 44.https://doi.org/10.1093/nar/gkw306
Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35(suppl_2):W407–W410. https://doi.org/10.1093/NAR/GKM290
Wood TM, McCrae SI, Bhat KM (1989) The mechanism of fungal cellulase action. Synergism between enzyme components of Penicillium pinophilum cellulase in solubilizing hydrogen bound-ordered cellulose. Biochem J 260(1):37–43. https://doi.org/10.1042/bj2600037
Xia T, Wang Q (2009) Directed evolution of Streptomyces lividans xylanase B toward enhanced thermal and alkaline pH stability. World J Microbiol Biotechnol 25(1):93–100. https://doi.org/10.1007/S11274-008-9867-3
Acknowledgements
The author would like to thank Tekirdağ Namık Kemal University for its contribution to the access to the full-text articles.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sürmeli, Y. Comparative investigation of bacterial thermoalkaliphilic GH11 xylanases at molecular phylogeny, sequence and structure level. Biologia 77, 3241–3253 (2022). https://doi.org/10.1007/s11756-022-01169-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-022-01169-6