Skip to main content
SpringerLink
Log in

Prebiotic effect of sorghum biomass xylooligosaccharides employing immobilized endoxylanase from Thermomyces lanuginosus PC7S1T

  • Biotechnology and Industrial Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Purified endoxylanase from Thermomyces lanuginosus PC7S1T was immobilized in calcium alginate, resulting in a yield of 78.5% and a reusability for 11 cycles. The stability of the immobilized enzyme was given for a pH range of 4 to 9 for 96 h. Endoxylanase immobilized in calcium alginate at 65 °C exhibited thermal stability equal to the soluble enzyme for 5 h, and at high temperatures of 75 °C and 85 °C showed half-lives of 4 and 3 h, respectively. Both soluble endoxylanase and immobilized forms were able to hydrolyze hemicellulose, obtained from low-lignin sorghum biomass pretreated with 5% H2O2 and 2% NaOH, after 1 h of incubation at 65 °C, releasing a mixture of short-chain xylooligosaccharides (X2–X6). The highest amounts of XOS generated were those for X5 (24 to 40%), X4 (33 to 39%), and X3 (11 to 22%). These XOS acted as prebiotics, promoting the growth of the probiotic L. acidophilus, similar to glucose in the MRS broth. These results show the potential of low-lignin sorghum to generate XOS with prebiotic activity, suggesting the application of these compounds in the food industry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Fernandes G, Braga TG, Fischer J, Parrella RAC, de Resende MM, Cardoso VL (2014) Evaluation of potential ethanol production and nutrients for four varieties of sweet sorghum during maturation. Renew Energy 71:518–524. https://doi.org/10.1016/j.renene.2014.05.033

    Article  CAS  Google Scholar 

  2. Rooney W, Blumenthal J, Bean BW, Mullet J (2007) Designing sorghum as a dedicated bioenergy feedstock. Biofuels Bioprod Biorefin 1(2):147–157. https://doi.org/10.1002/bbb.15

    Article  CAS  Google Scholar 

  3. de Almeida LGF, Parrella RAdaC, Simeone MLF, Ribeiro PCdeO, dos Santos AS, da Costa ASV, Guimarães AG, Schaffert RE (2019) Composition and growth of sorghum biomass genotypes for ethanol production. Biomass Bioenergy 122:343–348. https://doi.org/10.1016/j.biombioe.2019.01.030

    Article  CAS  Google Scholar 

  4. Oliveira ICM, Marçal TdeS, Bernardino KdaC, Ribeiro PCdeO, Parrella RAdaC, Carneiro PCS, Schaffert E, Carneiro JEdeS (2019) Combining ability of biomass sorghum lines for agroindustrial characters and multitrait selection of photosensitive hybrids for energy cogeneration. Crop Sci. 59:1554–1566. https://doi.org/10.2135/cropsci2018.11.0693

    Article  CAS  Google Scholar 

  5. da Silva DF, Garcia PHdeM, Santos GCdeL, de Farias IMS, de Pádua GVG, Pereira PHB, da Silva FE, Batista RF, Gonzaga Neto S, Cabral AMD (2021) Morphological characteristics genetic improvement and planting density of sorghum and corn crops a review. Res Soc Dev 10(3):e12310313172. https://doi.org/10.33448/rsd-v10i3.13172

    Article  Google Scholar 

  6. da Silva MJ, da Silva Júnior AC, Cruz CD, Nascimento M, Oliveira MdaS, Schaffert RE, Parrella RAdaC (2020) Computational intelligence for studies on genetic diversity between genotypes of biomass sorghum. Pesq. Agropec. Bras 55:e01723. https://doi.org/10.1590/S1678-3921.pab2020.v55.01723

    Article  Google Scholar 

  7. CONAB (2021) Companhia Nacional de Abastecimento. Acompanhamento da. safra brasileira de grãos. 8– Safra 2020/21, (12) - Décimo segundo levantamento, Brasília. 1–97, setembro 2021. Accessed 26 September 2021 Available from: https://www.conab.gov.br/infoagro/safras/graos/boletim-da-safra-de-grãos. Accessed 26 Sept 2021

  8. Guimarães CC, Simeone MLF, Parrella RAC, Sena MM (2014) Use of NIRS to predict composition and bioethanol yield from cell wall structural components of sweet sorghum biomass. Microchem J 117:194–201. https://doi.org/10.1016/j.microc.2014.06.029

    Article  CAS  Google Scholar 

  9. Della Torre CL, Silva-Lucca RA, Ferreira R, Luz LA, Oliva MLV, Kadowaki MK (2021) Correlation of the conformational structure and catalytic activity of the highly thermostable xylanase of Thermomyces lanuginosus PC7S1T. Biocatal. Biotransformation. https://doi.org/10.1080/10242422.2021.1950696

  10. de Freitas C, Terrone CC, Carmona EC, Brienzo M (2020) Evaluation of xylooligosaccharides effect on the growth of probiotic microorganisms. Braz J Dev 6(9):73400–73411. https://doi.org/10.34117/bjdv6n9-701

    Article  Google Scholar 

  11. Heinen PR, Bauermeister A, Ribeiro LF, Messias JM, Almeida PZ, Moraes LAB, Vargas-Rechia CG, de Oliveira AHC, Ward RJ, Filho EXF, Kadowaki MK, Jorge JA, Polizeli MLTM (2018) GH11 xylanase from Aspergillus tamarii Kita: purification by one-step chromatography and xylooligosaccharides hydrolysis monitored in real-time by mass spectrometry. Int J Biol Macromol 108:291–299. https://doi.org/10.1016/j.ijbiomac.2017.11.150

    Article  CAS  PubMed  Google Scholar 

  12. Bhushan B, Pal A, Jain V (2015) Improved enzyme catalytic characteristics upon glutaraldehyde cross-linking of alginate entrapped xylanase isolated from Aspergillus flavus MTCC9390. Enzyme Res 2015:210784. https://doi.org/10.1155/2015/210784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kuma RV, Chhabra D, Shukla P (2017) Xylanase production from Thermomyces lanuginosus VAPS-24 using low cost agro-industrial residues via hybrid optimization tools and its potential use for saccharification. Bioresour Technol 243:1009–1019. https://doi.org/10.1016/j.biortech.2017.07.094

    Article  CAS  Google Scholar 

  14. Kronbauer EAW, Peralta RM, Okaku CA, Kadowaki MM (2007) Xilanase production by Aspergillus casielus induced with different carbon sources. Bol Cent Pesq Process Aliment 25(2). https://doi.org/10.5380/cep.v25i2.10608

  15. Karlsson EN, Schmitz E, Pastén-Linares 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

    Article  CAS  Google Scholar 

  16. Park CS, Helmbrecht A, Htoo JK, Adeola O (2017) Comparison of amino acid digestibility in full-fat soybean, two soybean meals, and peanut flour between broiler chickens and growing pigs. J Anim Sci 95(7):3110–3119. https://doi.org/10.2527/jas.2017.1404

    Article  CAS  PubMed  Google Scholar 

  17. Bhatia R, Winters A, Bryant D, Bosch M, Clifton-Brown J, Leak D, Gallagher J (2020) Pilot-scale production of xylo-oligosaccharides and fermentable sugars from Miscanthus using steam explosion pretreatment. Bioresour Technol 296:122285. https://doi.org/10.1016/j.biortech.2019.122285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ghosh A, Sutradhar S, Baishya D. (2019) Delineating thermophilic xylanase from Bacillus licheniformis DM5 towards its potential application in xylooligosaccharides production. World J Microbiol Biotechnol 35(34). https://doi.org/10.1007/s11274-019-2605-1

  19. Amorim C, Silvério SC, Prather KLJ, Rodrigues LR (2019) From lignocellulosic residues to market: production and commercial potential of xylooligosaccharides. Biotechnol Adv 37(7):107397. https://doi.org/10.1016/j.biotechadv.2019.05.003

    Article  CAS  PubMed  Google Scholar 

  20. Ravichandra K, Balaji R, Devarapalli K, Batchu UR, Thadikamala S, Banoth L, Pinnamaneni SR, Prakasham RS (2022) Enzymatic production of prebiotic xylooligosaccharides from sorghum (Sorghum bicolor (L) xylan: value addition to sorghum bagasse. Biomass Conv Bioref. https://doi.org/10.1007/s13399-021-02216-z

    Article  Google Scholar 

  21. Santos-Rocha MSR, Souza RBA, Silva GM, Cruz AJG, Almeida RMRG (2017) Hydrothermal pretreatment of corn residues for second generation ethanol production. Sci Plena 13(3). https://doi.org/10.14808/sci.plena.2017.034202

  22. Corrêa JM, Christi D, Della Torre CL, Henn C, da Silva JLC, Kadowaki MK, de Simão RCG (2016) High levels of β-xylosidase in Thermomyces lanuginosus: potential use for saccharification. Braz. J. Microbiol. 47(3):680–690. https://doi.org/10.1016/j.bjm.2016.04.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31(3):426–428. https://doi.org/10.1021/ac60147a030

    Article  CAS  Google Scholar 

  24. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3

    Article  CAS  PubMed  Google Scholar 

  25. Silva JA, Macedo GP, Rodrigues DS, Giordano RL, Gonçalves LRB (2012) Immobilization of Candida antarctica lipase B by covalent attachment on chitosan-based hydrogels using different support activation strategies. Biochem Eng J 60:16–24. https://doi.org/10.1016/j.bej.2011.09.011

    Article  CAS  Google Scholar 

  26. McIlvaine TC (1921) A buffer solution for colorimetric comparison. J Biol Chem 49:185–186. https://doi.org/10.1016/S0021-9258(18)86000-8

    Article  Google Scholar 

  27. Menezes BS, Rossi DM, Squina F, Ayub MAZ (2018) Comparative production of xylanase and the liberation of xylooligosaccharides from lignocellulosic biomass by Aspergillus brasiliensis BLf1 and recombinant Aspergillus nidulans XynC A773. Int J Food Sci Technol 53(9):2110–2118. https://doi.org/10.1111/ijfs.13798

    Article  CAS  Google Scholar 

  28. Vinderola G, Prosello W, Molinari F, Ghiberto D, Reinheimer J (2009) Growth of Lactobacillus paracasei A13 in Argentinian probiotic cheese and its impact on the characteristics of the product. Int J Food Microbiol 135(2):171–174. https://doi.org/10.1016/j.ijfoodmicro.2009.08.021

    Article  CAS  PubMed  Google Scholar 

  29. Le B, Yang SH (2019) Production of prebiotic xylooligosaccharide from aqueous ammonia-pretreated rice straw by β-xylosidase of Weissella cibaria. J Appl Microbiol 126(6):1861–1868. https://doi.org/10.1111/jam.14255

    Article  CAS  PubMed  Google Scholar 

  30. Melati RB, Shimizu LF, Oliveira G, Pagnocca FC, Wde S, SantÀnna C, Brienzo M (2019) Key factors affecting the recalcitrance and conversion process of biomass. Bioenergy Res 12(1):1–20. https://doi.org/10.1007/s12155-018-9941-0

    Article  CAS  Google Scholar 

  31. Martins RP, Schmatz AA, de Freita LA, Mutton MJR, Brienzo M (2021) Solubilization of hemicellulose and fermentable sugars from bagasse, stalks, and leaves of sweet sorghum. Ind. Crops Prod. 170:113813. https://doi.org/10.1016/j.indcrop.2021.113813

    Article  CAS  Google Scholar 

  32. Assumpção SMN, Pontes LAM, de Carvalho LS, Campos LMA, de Andrade JCF, da Silva EG (2016) Pre-treatment combined H2SO4/H2O2/NaOH to obtain the lignocellulosic fractions of sugarcane bagasse. Rev. Virtual Quim. 8(3):803–822. https://doi.org/10.5935/1984-6835.20160059

    Article  Google Scholar 

  33. Kumar S, Haq I, Yadav A, Prakash J, Raj A (2016) Immobilization and biochemical properties of purified xylanase from Bacillus amyloliquefaciens SK-3 and its application in kraft pulp biobleaching. J Clin Microbiol Biochem Technol 2(1):026–034. https://doi.org/10.17352/jcmbt.000012

    Article  Google Scholar 

  34. Bibi Z, Qader SAU, Aman A (2015) Calcium alginate matrix increases the stability and recycling capability of immobilized endo-β-1,4-xylanase from Geobacillus stearothermophilus KIBGE-IB29. Extremophiles 19(4):819–827. https://doi.org/10.1007/s00792-015-0757-y

    Article  CAS  PubMed  Google Scholar 

  35. Rehman HU, Aman A, Silipo A, Qader SAU, Molinaro A, Ansari A (2013) Degradation of complex carbohydrate: immobilization of pectinase from Bacillus licheniformis KIBGE-IB21 using calcium alginate as a support. Food Chem 139(1–4):1081–1086. https://doi.org/10.1016/j.foodchem.2013.01.069

    Article  CAS  PubMed  Google Scholar 

  36. Kamal Kumar B, Balakrishnan H, Rele MV (2004) Compatibility of alkaline xylanases from an alkaliphilic Bacillus NCL (87–6-10) with commercial detergents and proteases. J Ind Microbiol Biotechnol 31:83–87. https://doi.org/10.1007/s10295-004-0119-8

    Article  CAS  PubMed  Google Scholar 

  37. Della Torre CL, Kadowaki MK (2017) Thermostable xylanase from thermophilic fungi: biochemical properties and industrial applications. Afr J Microbiol Res 11(2):28–37. https://doi.org/10.5897/AJMR2016.8361

    Article  CAS  Google Scholar 

  38. Wang X, Ma R, Xie X, Liu W, Tu T, Zheng F, You S, Ge J, Xie H, Yao B, Luo H (2017) Thermostability improvement of a Talaromyces leycettanus xylanase by rational protein engineering. Sci Rep 7(1):1–9. https://doi.org/10.1038/s41598-017-12659-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Walia A, Guleria S, Mehta P, Chauhan A, Parkash J (2017) Microbial xylanases and their industrial application in pulp and paper biobleaching: a review. 3 Biotech. 7(1):11. https://doi.org/10.1007/s13205-016-0584-6

    Article  PubMed  PubMed Central  Google Scholar 

  40. Quiñones TS, Retter A, Hobbs PJ, Budde J, Heiermann M, Plöch M, Ravella SR (2015) Production of xylooligosaccharides from renewable agricultural lignocellulose biomass. Biofuels 6(3–4):147–155. https://doi.org/10.1080/17597269.2015.1065589

    Article  CAS  Google Scholar 

  41. Milessi TS, Corradini FAS, Marçal JVM, Baldez TO, Kopp W, Giordano RC, Giordano RLC (2021) Xylooligosaccharides production chain in sugarcane biorefineries: from the selection of pretreatment conditions to the evaluation of nutritional properties. Ind. Crops Prod. 172:114056. https://doi.org/10.1016/j.indcrop.2021.114056

    Article  CAS  Google Scholar 

  42. PdeO R, JdeC P, Santos DQ, Gurgel LVA, Pasquini D, Baffi MA (2017) Synergistic action of an Aspergillus (hemi-)cellulolytic consortium on sugarcane bagasse saccharification. Ind Crops Prod 109:173–181. https://doi.org/10.1016/j.indcrop.2017.08.031

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Érica S. Zuppa and Maiara Zonin are recipient of fellowship from Fundação Araucária and National Council for Scientific and Technological Development (CNPq), respectively. Diandra de Andrades is recipient of fellowship from Coordination of Improvement of Higher Education Personnel (CAPES)-Brazil.

Author information

Authors and Affiliations

  1. Center of Medical Sciences and Pharmaceutical, Western Paraná State University, Rua Universitária, 2069, Cascavel, PR, ZC 85814-110, Brazil

    Andreza Gambelli Lucas Costa Nascimento, Érica Sabrina Zuppa, Maiara Zonin, Gabriela Furlaneto Sanchez de Sousa, Alexandre Maller, José Luis da Conceição Silva, Rita de Cássia Garcia Simão & Marina Kimiko Kadowaki

  2. Biotechnology Bioprocess and Biocatalysis Group, Food Science and Technology Institute, Federal University of Rio Grande Do Sul, Av. Bento Gonçalves 9500, PO Box 15090, Porto Alegre, RS, ZC 91501-970, Brazil

    Diandra de Andrades & Marco Antônio Záchia Ayub

Authors
  1. Andreza Gambelli Lucas Costa Nascimento
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Érica Sabrina Zuppa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maiara Zonin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriela Furlaneto Sanchez de Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Diandra de Andrades
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marco Antônio Záchia Ayub
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alexandre Maller
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. José Luis da Conceição Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rita de Cássia Garcia Simão
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marina Kimiko Kadowaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marina Kimiko Kadowaki.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Inês Conceição Roberto

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nascimento, A., Zuppa, É., Zonin, M. et al. Prebiotic effect of sorghum biomass xylooligosaccharides employing immobilized endoxylanase from Thermomyces lanuginosus PC7S1T. Braz J Microbiol 53, 1167–1174 (2022). https://doi.org/10.1007/s42770-022-00754-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-022-00754-w

Keywords

Search

Navigation