Xylanolytic Bacillus species for xylooligosaccharides production: a critical review

Abstract

The capacity of different Bacillus species to produce large amounts of extracellular enzymes and ability to ferment various substrates at a wide range of pH and temperature has placed them among the most promising hosts for the industrial production of many improved and novel products. The global interest in prebiotics, for example, xylooligosaccharides (XOs) is ever increasing, rousing the quest for various forms with expanded productivity. This article provides an overview of xylanase producing bacilli, with more emphasis on their capacity to be used in the production of the XOs, followed by the purification strategies, characteristics and application of XOs from bacilli. The large-scale production of XOs is carried out from a number of xylan-rich lignocellulosic materials by chemical or enzymatic hydrolysis followed by purification through chromatography, vacuum evaporation, solvent extraction or membrane separation methods. Utilization of XOs in the production of functional products as food ingredients brings well-being to individuals by improving defense system and eliminating pathogens. In addition to the effects related to health, a variety of other biological impacts have also been discussed.

Keywords

Bacillus / Prebiotics / Xylanase / Xylooligosaccharides

References

[1] Aachary AA, Prapulla SG. Xylooligosaccharides (XOS) as an emerging prebiotic: microbial synthesis, utilization, structural characterization, bioactive properties, and applications. Compr Rev Food Sci Food Saf, 2011, 10: 2-16.

[2] Aarti C, Arasu MV, Agastian P. Lignin Degradation: a Microbial Approach. South Indian J Biol Sci, 2015, 1: 119-127.

[3] Akhavan Sepahy A, Ghazi S, Akhavan Sepahy M. Cost-effective production and optimization of alkaline xylanase by indigenous Bacillus mojavensis AG137 fermented on agricultural waste. Enzyme Res, 2011

[4] Akpinar O, Ak O, Kavas A, . Enzymatic production of xylooligosaccharides from cotton stalks. J Agric Food Chem, 2007, 55: 5544-5551.

[5] Akpinar O, Erdogan K, Bakir U, Yilmaz L. Comparison of acid and enzymatic hydrolysis of tobacco stalk xylan for preparation of xylooligosaccharides. LWT-Food Sci Technol, 2010, 43: 119-125.

[6] Amore A, Parameswaran B, Kumar R, . Application of a new xylanase activity from Bacillus amyloliquefaciens XR44A in brewer’s spent grain saccharification. J Chem Technol Biotechnol, 2015, 90: 573-581.

[7] Amorim C, Silvério SC, Gonçalves RFS, . Downscale fermentation for xylooligosaccharides production by recombinant Bacillus subtilis 3610. Carbohydr Polym, 2019, 205: 176-183.

[8] Anand L, Krishnamurthy S, Vithayathil PJ. Purification and properties of xylanase from the thermophilic fungus, Humicola lanuginosa (Griffon and Maublanc) Bunce. Arch Biochem Biophys, 1990, 276: 546-553.

[9] Ando H, Ohba H, Sakaki T, . Hot-compressed-water decomposed products from bamboo manifest a selective cytotoxicity against acute lymphoblastic leukemia cells. Toxicol Vitr, 2004, 18: 765-771.

[10] Arai T, Biely P, Uhliariková I, . Structural characterization of hemicellulose released from corn cob in continuous flow type hydrothermal reactor. J Biosci Bioeng, 2019, 127: 222-230.

[11] Avcioglu B, Eyupoglu B, Bakir U. Production and characterization of xylanases of a Bacillus strain isolated from soil. World J Microbiol Biotechnol, 2005, 21: 65-68.

[12] Ayishal Begam M, Annu A, Shameera Banu S, Vishnu Priya D. Comparison and optimization of thermostable xylanase production by bacillus pumilus and bacillus cereus using corn husk. Iarjset, 2015, 9: 139-147.

[13] Bajpai P (2014) Microbial Xylanolytic Systems and Their Properties. In: Xylanolytic Enzymes. pp 19–36

[14] Bakri Y, Ammouneh H, Harba M, . Xylanase production by a new bacillus pumilus SY30A under solid state fermentation and its application in oil palm biomass pulp bleaching. J Sustain Sci Manag, 2016, 11: 1-8.

[15] Bernardeau M, Lehtinen MJ, Forssten SD, Nurminen P. Importance of the gastrointestinal life cycle of Bacillus for probiotic functionality. J Food Sci Technol., 2017, 54: 2570-2584.

[16] Bhardwaj N, Kumar B, Verma P. A detailed overview of xylanases: an emerging biomolecule for current and future prospective. Bioresour Bioprocess., 2019, 6: 40.

[17] Bian J, Peng P, Peng F, . Microwave-assisted acid hydrolysis to produce xylooligosaccharides from sugarcane bagasse hemicelluloses. Food Chem, 2014, 156: 7-13.

[18] Bocchini DA, Gomes E, Da Silva R (2007) Xylanase Production by Bacillus circulans D1 Using Maltose as Carbon Source. In: Biotechnology for Fuels and Chemicals. pp 149–157

[19] Bragatto J, Segato F, Squina FM. Production of xylooligosaccharides (XOS) from delignified sugarcane bagasse by peroxide-HAc process using recombinant xylanase from Bacillus subtilis. Ind Crops Prod, 2013, 51: 123-129.

[20] Breccia JD, Siñeriz F, Baigorí MD, . Purification and characterization of a thermostable xylanase from Bacillus amyloliquefaciens. Enzyme Microb Technol, 1998, 22: 42-59.

[21] Brienzo M, Carvalho W, Milagres AMF. Xylooligosaccharides production from alkali-pretreated sugarcane bagasse using xylanases from Thermoascus aurantiacus. Appl Biochem Biotechnol, 2010, 162: 1195-1205.

[22] Broekaert W. Christophe C. Jan D (2011) (arabino)xylan oligosaccharide preparation. US20110020498A1

[23] Bron S, Meima R, Van Dijl JM, . Molecular Biology and Genetics of Bacillus species. Man Ind Microbiol Biotechnol, 1999, 7: 4-49.

[24] Budhathoki U, Thapa P, Poluri E. Medium optimization of production of xylanase by solid state fermentation from Brevibacillus borstelensis-MTCC 9874 isolated from soil sample of eastern Nepal. Malays J Microbiol, 2011, 7: 83-91.

[25] Cano À, Palet C. Xylooligosaccharide recovery from agricultural biomass waste treatment with enzymatic polymeric membranes and characterization of products with MALDI-TOF-MS. J Memb Sci, 2007, 291: 96-105.

[26] Chadha BS, Kaur B, Basotra N, . Thermostable xylanases from thermophilic fungi and bacteria: current perspective. Bioresour Technol., 2019, 277: 195-203.

[27] Chakdar H, Kumar M, Pandiyan K, . Bacterial xylanases: biology to biotechnology. 3 Biotech, 2016, 6: 1-15.

[28] Chapla D, Pandit P, Shah A. Production of xylooligosaccharides from corncob xylan by fungal xylanase and their utilization by probiotics. Bioresour Technol, 2012, 115: 215-221.

[29] Chauhan S, Seth CA, Seth A. Bioprospecting thermophilic microorganisms from hot springs of western Himalayas for xylanase production and its statistical optimization by using response surface methodology. J Pure Appl Microbiol, 2015, 9: 1417-1428.

[30] Chen HH, Chen YK, Chang HC, Lin SY. Immunomodulatory effects of xylooligosaccharides. Food Sci Technol Res, 2012, 18: 195-199.

[31] Christakopoulos P, Katapodis P, Kalogeris E, . Antimicrobial activity of acidic xylo-oligosaccharides produced by family 10 and 11 endoxylanases. Int J Biol Macromol, 2003, 31: 171-175.

[32] Collins T, Gerday C, Feller G. Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol. Rev., 2005, 29: 3-23.

[33] Crittenden R, Karppinen S, Ojanen S, . In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria. J Sci Food Agric, 2002, 82: 781-789.

[34] Dahlberg L, Holst O, Kristjansson JK. Thermostable xylanolytic enzymes from Rhodothermus marinus grown on xylan. Appl Microbiol Biotechnol, 1993, 40: 63-68.

[35] Davani-Davari D, Negahdaripour M, Karimzadeh I, . Prebiotics: Definition, types, sources, mechanisms, and clinical applications. Foods, 2019, 8: 92.

[36] de Oliva-Neto P, Menão PTP. Isomaltulose production from sucrose by Protaminobacter rubrum immobilized in calcium alginate. Bioresour Technol, 2009, 100: 4252-4256.

[37] de Freitas C, Carmona E, Brienzo M. Xylooligosaccharides production process from lignocellulosic biomass and bioactive effects. Bioact Carbohydrates Diet Fibre, 2019, 18: 100184.

[38] Deka D, Das SP, Sahoo N, . Enhanced cellulase production from bacillus subtilis by optimizing physical parameters for bioethanol production. ISRN Biotechnol, 2013

[39] Dorta C, Cruz R, De Oliva-Neto P, Moura DJC. Sugarcane molasses and yeast powder used in the Fructooligosaccharides production by Aspergillus japonicus-FCL 119T and Aspergillus niger ATCC 20611. J Ind Microbiol Biotechnol, 2006, 33: 1003.

[40] Elshaghabee FMF, Rokana N, Gulhane RD, . Bacillus as potential probiotics: Status, concerns, and future perspectives. Front Microbiol., 2017, 8: 1490.

[41] Finegold SM, Li Z, Summanen PH, . Xylooligosaccharide increases bifidobacteria but not lactobacilli in human gut microbiota. Food Funct, 2014, 5: 436-445.

[42] Freixo MR, De Pinho MN. Enzymatic hydrolysis of beechwood xylan in a membrane reactor. Desalination, 2002, 149: 237-242.

[43] Gabrielii I, Gatenholm P. Preparation and properties of hydrogels based on hemicellulose. J Appl Polym Sci, 1998, 69: 1661-1667.

[44] Gallardo Ó, Fernández-Fernández M, Valls C, . Characterization of a family GH5 xylanase with activity on neutral oligosaccharides and evaluation as a pulp bleaching aid. Appl Environ Microbiol, 2010, 76: 6290-6294.

[45] Geetha K, Gunasekaran P. Purification of endoxylanase from bacillus pumilus B20 for production of prebiotic xylooligosaccharide syrup; An in vitro study. Iran J Biotechnol, 2017, 15: 232.

[46] Gibson GR, Scott KP, Rastall RA, . Dietary prebiotics: current status and new definition. Food Sci Technol Bull Funct Foods, 2010, 7: 1-19.

[47] Gimenez GG, Costa H, de Lima Neto QA, . Sequencing, cloning, and heterologous expression of cyclomaltodextrin glucanotransferase of Bacillus firmus strain 37 in Bacillus subtilis WB800. Bioprocess Biosyst Eng, 2019, 42: 621-629.

[48] Glasser WG, Jain RK, Sjostedt MA (1995) Thermoplastic pentosan-rich polysaccharides from biomass. U.S. Patent No. 5,430,142

[49] Goswami GK, Krishnamohan M, Nain V, . Cloning and heterologous expression of cellulose free thermostable xylanase from Bacillus brevis. Springerplus, 2014, 3: 20.

[50] Gowdhaman D, Manaswini VS, Jayanthi V, . Xylanase production from Bacillus aerophilus KGJ2 and its application in xylooligosaccharides preparation. Int J Biol Macromol, 2014, 64: 90-98.

[51] Grootaert C, Verstraete W, Van de Wiele T. Arabinoxylan oligosaccharides with different structures exert a bifidogenic effect in a mixed intestinal community. Commun Agric Appl Biol Sci, 2006, 71: 159-163.

[52] Guo Y, Gao Z, Xu J, . A family 30 glucurono-xylanase from Bacillus subtilis LC9: expression, characterization and its application in Chinese bread making. Int J Biol Macromol, 2018, 117: 377-384.

[53] Haddar A, Driss D, Frikha F, . Alkaline xylanases from Bacillus mojavensis A21: production and generation of xylooligosaccharides. Int J Biol Macromol, 2012, 51: 647-656.

[54] Ho AL, Carvalheiro F, Duarte LC, . Production and purification of xylooligosaccharides from oil palm empty fruit bunch fibre by a non-isothermal process. Bioresour Technol, 2014, 152: 526-529.

[55] Holck J, Hotchkiss AT, Meyer AS, et al (2014) Production and Bioactivity of Pectic Oligosaccharides from Fruit and Vegetable Biomass. In: Food Oligosaccharides: production, analysis and bioactivity. pp 76–87

[56] Irfan M, Nadeem M, Syed Q, Baig S. Effect of medium composition on Xylanase production by bacillus subtilis using various agricultural wastes. J Agric Environ Sci, 2012, 12: 561-565.

[57] Jagtap S, Deshmukh RA, Menon S, Das S. Xylooligosaccharides production by crude microbial enzymes from agricultural waste without prior treatment and their potential application as nutraceuticals. Bioresour Technol, 2017, 245: 283-288.

[58] Jain M, Gupta K, Jain P. Significance of probiotics and prebiotics in health and nutrition. Malaya J Biosci, 2014, 1: 181-195.

[59] Jaskari J, Kontula P, Siitonen A, . Oat β-glucan and xylan hydrolysates as selective substrates for Bifidobacterium and Lactobacillus strains. Appl Microbiol Biotechnol, 1998, 49: 175-181.

[60] John FJ, Rice JD, Preston JF. Characterization of XynC from Bacillus subtilis subsp. subtilis strain 168 and analysis of its role in depolymerization of glucuronoxylan. J Bacteriol, 2006

[61] Kabel MA, Kortenoeven L, Schols HA, Voragen AGJ. In vitro fermentability of differently substituted xylo-oligosaccharides. J Agric Food Chem, 2002, 50: 6205-6210.

[62] Kademi A, Ait-Abdelkader N, Fakhreddine L, Baratti J. Purification and characterization of a thermostable esterase from the moderate thermophile Bacillus circulans. Appl Microbiol Biotechnol, 2000, 54: 173-179.

[63] Kallel F, Driss D, Bouaziz F, . Production of xylooligosaccharides from garlic straw xylan by purified xylanase from Bacillus mojavensis UEB-FK and their in vitro evaluation as prebiotics. Food Bioprod Process, 2015, 94: 536-546.

[64] Kaprelyants L, Zhurlova O, Shpyrko T, Pozhitkova L. Xylooligosaccharides from agricultural by-products: characterisation, production and physiological effects. Food Sci Technol, 2017, 11: 25-34.

[65] Karnaouri A, Matsakas L, Krikigianni E, . Valorization of waste forest biomass toward the production of cello-oligosaccharides with potential prebiotic activity by utilizing customized enzyme cocktails. Biotechnol Biofuels, 2019, 12: 285.

[66] Khat-udomkiri N, Toejing P, Sirilun S, . Antihyperglycemic effect of rice husk derived xylooligosaccharides in high-fat diet and low-dose streptozotocin-induced type 2 diabetic rat model. Food Sci Nutr, 2020, 8: 428-444.

[67] Khusro A, Kaliyan BK, Al-Dhabi NA, . Statistical optimization of thermo-alkali stable xylanase production from Bacillus tequilensis strain ARMATI. Electron J Biotechnol, 2016, 22: 16-25.

[68] Ko CH, Shih TL, Jhan BT, . Production of xylooligosaccharides from forest waste by membrane separation and Paenibacillus xylanase hydrolysis. BioResources, 2013, 8: 612-627.

[69] Kobayashi T, Fujikawa S, Koga K, Okazaki M. Effect of Xylooligosaccharides on Feces of Men. Nippon Nogeikagaku Kaishi, 1991, 65: 1651-1653.

[70] Kumar V, Satyanaana T. Production of thermo-alkali-stable xylanase by a novel polyextremophilic Bacillus halodurans TSEV1 in cane molasses medium and its applicability in making whole wheat bread. Bioprocess Biosyst Eng, 2014, 37: 1043-1053.

[71] Le B, Ngoc APT, Yang SH. Synbiotic fermented soymilk with Weissella cibaria FB069 and xylooligosaccharides prevents proliferation in human colon cancer cells. J Appl Microbiol, 2020, 128: 1486-1496.

[72] Lim SM, Kim E, Shin JH, . Xylobiose prevents high-fat diet induced mice obesity by suppressing mesenteric fat deposition and metabolic dysregulation. Molecules, 2018, 23: 705.

[73] Lin YS, Tseng MJ, Lee WC. Production of xylooligosaccharides using immobilized endo-xylanase of Bacillus halodurans. Process Biochem, 2011, 46: 2117-2121.

[74] Lin SH, Chou LM, Chien YW, . Prebiotic Effects of Xylooligosaccharides on the improvement of microbiota balance in human subjects. Gastroenterol Res Pract, 2016

[75] Liu MQ, Liu GF. Expression of recombinant Bacillus licheniformis xylanase A in Pichia pastoris and xylooligosaccharides released from xylans by it. Protein Expr Purif, 2008, 57: 101-107.

[76] Liu qi M, Huo kang W, Xu X, Weng yan X. Recombinant Bacillus amyloliquefaciens xylanase A expressed in Pichia pastoris and generation of xylooligosaccharides from xylans and wheat bran. Int J Biol Macromol, 2017, 105: 656-663.

[77] Lombard V, Golaconda Ramulu H, Drula E, . The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res, 2014, 42: 490-495.

[78] Maehara T, Yagi H, Sato T, . GH30 glucuronoxylan-specific xylanase from Streptomyces turgidiscabies C56. Appl Environ Microbiol, 2018

[79] Mäkeläinen H, Juntunen M, Hasselwander O (2009) Prebiotic Potential of Xylo-Oligosaccharides. In: Prebiotics and Probiotics Science and Technology. p 245

[80] Mamo G, Hatti-Kaul R, Mattiasson B. A thermostable alkaline active endo-β-1-4-xylanase from Bacillus halodurans S7: Purification and characterization. Enzyme Microb Technol, 2006, 39: 1492-1498.

[81] Marín-Manzano MC, Abecia L, Hernández-Hernández O, . Galacto-oligosaccharides derived from lactulose exert a selective stimulation on the growth of bifidobacterium animalis in the large intestine of growing rats. J Agric Food Chem, 2013, 61: 7560-7567.

[82] Mathew S, Aronsson A, Karlsson EN, Adlercreutz P. Xylo- and arabino-xylooligosaccharides from wheat bran by endoxylanases, utilisation by probiotic bacteria, and structural studies of the enzymes. Appl Microbiol Biotechnol, 2018, 102: 3105-3120.

[83] Míguez B, Gómez B, Gullón P, et al (2016) Pectic Oligosaccharides and Other Emerging Prebiotics. In: Probiotics and Prebiotics in Human Nutrition and Health. pp 301–330

[84] Milessi TSS, Kopp W, Rojas MJ, . Immobilization and stabilization of an endoxylanase from Bacillus subtilis (XynA) for xylooligosaccharides (XOs) production. Catal Today, 2016, 259: 130-139.

[85] Mondal KC, Banerjee R, Pati BR. Tannase production by Bacillus licheniformis. Biotechnol Lett, 2000, 22: 767-769.

[86] Moreira LRS, Filho EXF. Insights into the mechanism of enzymatic hydrolysis of xylan. Appl Microbiol Biotechnol., 2016, 100: 5205-5214.

[87] Motta FL, Andrade CC, Santana MH (2013) A Review of Xylanase Production by the Fermentation of Xylan: classification, characterization and applications. In: Sustainable Degradation of Lignocellulosic Biomass-Techniques, Applications and Commercialization

[88] Moure A, Gullón P, Domínguez H, Parajó JC. Advances in the manufacture, purification and applications of xylo-oligosaccharides as food additives and nutraceuticals. Process Biochem., 2006, 41: 1913-1923.

[89] Nabarlatz D, Farriol X, Montané D. Kinetic modeling of the autohydrolysis of lignocellulosic biomass for the production of hemicellulose-derived oligosaccharides. Ind Eng Chem Res, 2004, 43: 4124-4131.

[90] Nabarlatz D, Torras C, Garcia-Valls R, Montané D. Purification of xylo-oligosaccharides from almond shells by ultrafiltration. Sep Purif Technol, 2007, 53: 235-243.

[91] Nagar S, Jain RK, Thakur VV, Gupta VK. Biobleaching application of cellulase poor and alkali stable xylanase from Bacillus pumilus SV-85S. 3 Biotech, 2013, 3: 277-285.

[92] Nakamura S, Wakabayashi K, Nakai R, . Purification and some properties of an alkaline xylanase from alkaliphilic Bacillus sp. strain 41M–1. Appl Environ Microbiol, 1993

[93] Naseeb S, Sohail M, Ahmad A, Khan SA. Production of xylanases and cellulases by aspergillus fumigatus ms16 using crude lignocellulosic substrates. Pakistan J Bot, 2015, 47: 779-784.

[94] Ohbuchi T, Takahashi T, Azumi N, Sakaino M. Structural analysis of neutral and acidic xylooligosaccharides from hardwood kraft pulp, and their utilization by intestinal bacteria in vitro. Biosci Biotechnol Biochem, 2009, 73: 2070-2076.

[95] Okazaki M, Fujikawa S, Matsumoto N. Effect of Xylooligosaccharide on the growth of Bifidobacteria. Bifidobact Microflora, 1990, 9: 77-86.

[96] Olaimat AN, Aolymat I, Al-Holy M, . The potential application of probiotics and prebiotics for the prevention and treatment of COVID-19. npj. Sci Food, 2020, 4: 1-7.

[97] Pan J, Yin J, Zhang K, . Dietary xylo-oligosaccharide supplementation alters gut microbial composition and activity in pigs according to age and dose. AMB Express, 2019, 9: 1-10.

[98] Pellerin P, Gosselin M, Lepoutre JP, . Enzymic production of oligosaccharides from corncob xylan. Enzyme Microb Technol, 1991, 13: 617-621.

[99] Perez Oseguera MA, Guereca L, Lopez-Munguia A. Properties of levansucrase from Bacillus circulans. Appl Microbiol Biotechnol, 1996, 45: 465-471.

[100] Pinelo M, Jonsson G, Meyer AS. Membrane technology for purification of enzymatically produced oligosaccharides: molecular and operational features affecting performance. Sep Purif Technol., 2009, 70: 1-11.

[101] Poletto P, Pereira GN, Monteiro CRM, . Xylooligosaccharides: Transforming the lignocellulosic biomasses into valuable 5-carbon sugar prebiotics. Process Biochem., 2020, 91: 352-363.

[102] Oakley AJ, Heinrich T, Thompson CA, Wilce MCG. Characterization of a family 11 xylanase from Bacillus subtilis B230 used for paper bleaching. Act Cryst, 2003, 59: 627-636.

[103] Qi B, Luo J, Chen G, . Application of ultrafiltration and nanofiltration for recycling cellulase and concentrating glucose from enzymatic hydrolyzate of steam exploded wheat straw. Bioresour Technol, 2012, 104: 466-472.

[104] Qing Q, Li H, Kumar R, Wyman CE (2013) Xylooligosaccharides Production, Quantification, and Characterization in Context of Lignocellulosic Biomass Pretreatment. In: Aqueous Pretreatment of Plant Biomass for Biological and Chemical Conversion to Fuels and Chemicals. pp 391–415

[105] Quiñones TS, Retter A, Hobbs PJ, . Production of xylooligosaccharides from renewable agricultural lignocellulose biomass. Biofuels, 2015, 6: 147-155.

[106] Reddy SS, Krishnan C. Production of xylooligosaccharides in SSF by Bacillus subtilis KCX006 producing β-xylosidase-free endo-xylanase and multiple xylan debranching enzymes. Prep Biochem Biotechnol, 2016, 46: 49-55.

[107] Reddy SS, Krishnan C. Production of high-pure xylooligosaccharides from sugarcane bagasse using crude β-xylosidase-free xylanase of Bacillus subtilis KCX006 and their bifidogenic function. LWT-Food Sci Technol, 2016, 65: 237-245.

[108] Regmi S, Pradeep GC, Choi YH, . A multi-tolerant low molecular weight mannanase from Bacillus sp. CSB39 and its compatibility as an industrial biocatalyst. Enzyme Microb Technol, 2016, 92: 76-85.

[109] Rehman S, Aslam H, Ahmad A, . Production of plant cell wall degrading enzymes by monoculture and co-culture of Aspergillus niger and Aspergillus terreus under SSF of banana peels. Brazilian J Microbiol, 2014, 1492: 1485-1492.

[110] Reque PM, Pinilla CMB, Gautério GV, . Xylooligosaccharides production from wheat middlings bioprocessed with Bacillus subtilis. Food Res Int, 2019, 126: 108673.

[111] Sako T, Tanaka R (2011) Prebiotics: types. In: encyclopedia of dairy sciences: Second Edition

[112] Samanta AK, Jayapal N, Jayaram C, . Xylooligosaccharides as prebiotics from agricultural by-products: production and applications. Bioact Carbohydrates Diet Fibre, 2015, 5: 62-71.

[113] Schallmey M, Singh A, Ward OP. Developments in the use of Bacillus species for industrial production. Can. J. Microbiol., 2004, 50: 1-17.

[114] Selvarajan E, Veena R. Recent advances and future perspectives of thermostable xylanase. Biomed Pharmacol J., 2017, 10: 261-279.

[115] Shariq M, Sohail M. Application of Candida tropicalis MK-160 for the production of xylanase and ethanol. J King Saud Univ - Sci, 2018, 31: 1189-1194.

[116] Shimoda K, Hamada H, Hamada H. Synthesis of xylooligosaccharides of daidzein and their anti-oxidant and anti-allergic activities. Int J Mol Sci, 2011, 12: 5616-5625.

[117] Shrinivas D, Savitha G, Raviranjan K, Naik GR. A highly thermostable alkaline cellulase-free xylanase from thermoalkalophilic bacillus sp. JB 99 suitable for paper and pulp industry: purification and characterization. Appl Biochem Biotechnol, 2010, 162: 2049-2057.

[118] Singh S, Bajaj BK. Potential application spectrum of microbial proteases for clean and green industrial production. Energy Ecol Environ., 2017, 2: 370-386.

[119] Sohail M, Ahmad A, Shahzad S, Khan SA. A survey of amylolytic bacteria and fungi from native environmental samples. Pakistan J Bot, 2005, 37: 155-161.

[120] Sohail M, Naseeb S, Sherwani SK, . Distribution of hydrolytic enzymes among native fungi: Aspergillus the pre-dominant genus of hydrolase producer. Pakistan J Bot, 2009, 41: 2567-2582.

[121] Subramaniyan S. Isolation, purification and characterisation of low molecular weight xylanase from Bacillus pumilus SSP-34. Appl Biochem Biotechnol, 2012, 166: 1831-1842.

[122] Subramaniyan S, Prema P. Biotechnology of microbial xylanases: enzymology, molecular biology, and application. Crit Rev Biotechnol., 2002, 22: 33-64.

[123] Suwa, Yoshihide ; Koga, Kunimasa ; Fujikawa, Shigeaki ; Okazaki, Masako ; Irie, Toshio; Nakada T (1999) Bifidobacterium bifidum proliferation promoting composition containing xylooligosaccharide. J Can Dent Assoc.

[124] Tateyama I, Hashii K, Johno I, . Effect of xylooligosaccharide intake on severe constipation in pregnant women. J Nutr Sci Vitaminol, 2005, 51: 445-448.

[125] Thamthiankul S, Suan-Ngay S, Tantimavanich S, Panbangred W. Chitinase from Bacillus thuringiensis subsp. pakistani. Appl Microbiol Biotechnol, 2001, 56: 395-401.

[126] Turck D, Bresson JL, Burlingame B, . Safety of xylo-oligosaccharides (XOS) as a novel food pursuant to regulation (EU) 2015/2283. EFSA J, 2018

[127] Vázquez MJ, Alonso JL, Domínguez H, Parajó JC. Xylooligosaccharides: manufacture and applications. Trends Food Sci Technol, 2000, 11: 387-393.

[128] Vegas R, Alonso JL, Domínguez H, Parajó JC. Manufacture and refining of oligosaccharides from industrial solid wastes. Ind Eng Chem Res, 2005, 44: 614-620.

[129] Verma D, Satyanarayana T. Cloning, expression and applicability of thermo-alkali-stable xylanase of Geobacillus thermoleovorans in generating xylooligosaccharides from agro-residues. Bioresour Technol, 2012, 107: 333-338.

[130] Vršanská M, Kolenová K, Puchart V, Biely P. Mode of action of glycoside hydrolase family 5 glucuronoxylan xylanohydrolase from Erwinia chrysanthemi. FEBS J, 2007, 274: 1666-1677.

[131] Walia A, Guleria S, Mehta P, . Microbial xylanases and their industrial application in pulp and paper biobleaching: a review. Biotech, 2017, 7: 11.

[132] Wan Azelee NI, Jahim JM, Ismail AF, . High xylooligosaccharides (XOS) production from pretreated kenaf stem by enzyme mixture hydrolysis. Ind Crops Prod, 2016, 81: 11-19.

[133] Wang Y, Cao X, Zhang R, . Evaluation of xylooligosaccharide production from residual hemicelluloses of dissolving pulp by acid and enzymatic hydrolysis. RSC Adv, 2018, 8: 35211-35217.

[134] Wang K, Cao R, Wang M, . 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, 2019, 12: 48.

[135] Wijaya H, Sasaki K, Kahar P, . High enzymatic recovery and purification of xylooligosaccharides from empty fruit bunch via nanofiltration. Processes, 2020, 8: 615.

[136] Xu F, Chen J, Yang G, . Combined treatments consisting of calcium hydroxide and activate carbon for purification of xylo-oligosaccharides of pre-hydrolysis liquor. Polymers, 2019, 11: 1558.

[137] Yadav P, Maharjan J, Korpole S, . Production, purification, and characterization of thermostable alkaline xylanase from Anoxybacillus kamchatkensis NASTPD13. Front Bioeng Biotechnol, 2018, 6: 65.

[138] Yang J, Summanen PH, Henning SM, . Xylooligosaccharide supplementation alters gut bacteria in both healthy and prediabetic adults: a pilot study. Front Physiol, 2015, 6: 216.

[139] Yuan QP, Zhang H, Qian ZM, Yang XJ. Pilot-plant production of xylo-oligosaccharides from corncob by steaming, enzymatic hydrolysis and nanofiltration. J Chem Technol Biotechnol, 2004, 79: 1073-1079.

[140] Zeldes BM, Keller MW, Loder AJ, . Extremely thermophilic microorganisms as metabolic engineering platforms for production of fuels and industrial chemicals. Front Microbiol., 2015, 6: 1209.

[141] Zhang S, Wang C, Sun Y, . Xylanase and fermented polysaccharide of Hericium caputmedusae reduce pathogenic infection of broilers by improving antioxidant and anti-Inflammatory properties. Oxid Med Cell Longev, 2018

[142] Zhao X, Dong C. Extracting xylooligosaccharides in wheat bran by screening and cellulase assisted enzymatic hydrolysis. Int J Biol Macromol, 2016, 92: 748-752.

Funding

Higher Education Commission, Pakistan(AHBP Program)