Biovalorization of the raw agro-industrial waste rice husk through directed production of xylanase by Thermomyces lanuginosus strain A3-1 DSM 105773: a statistical sequential model

Abstract

The current work addresses a statistically optimized, economic, and efficient approach for the professional valorization of the massively accumulated non-efficiently utilized, raw agro-industrial waste rice husk (RH). Thermomyces lanuginosus strain A3-1 DSM 105773, a locally isolated strain, was employed for directed production of xylanase, an industrially important enzyme upon growing on RH-based medium. A three-step empirical sequential, statistical approach—one variable at a time (OVAT), Plackett–Burman design (PBD), and Box–Behnken design (BBD)—was employed to optimize the xylanase production through liquid-state fermentation of rice husk. Incubation temperature (50 °C) and ammonium sulfate concentration as an inorganic nitrogen source were the most appropriate parameters triggering the production of xylanase, deduced from OVAT. The three key determinants RH concentration, initial pH of the production medium, and incubation time did exhibit significant influences (P ≤ 0.001) on the production of xylanase, deduced from PBD. By the end of the optimization process, the optimal levels of RH, initial pH of the production medium, and incubation time were 3.8% (w/v), 4.5, and 8 days, respectively, with an agitation speed of 120 rpm to achieve a maximal xylanase level of 0.8344 U/mL with a fivefold enhancement deduced from the estimated ridge of the canonical path. Present data would reinforce the scaling up of xylanase production using the present powerful and reproducible approach for the simultaneous and proficient valorization of RH and production of xylanase for further exploitation in food, pharmaceutical, and textile industries.

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References

  1. 1.

    Howard RL, Abotsi ELJR, Van Rensburg EJ, Howard S (2003) Lignocellulose biotechnology: issues of bioconversion and enzyme production. African J Biotechnol 2:602–619

    Google Scholar 

  2. 2.

    Pothiraj C, Kanmani P, Balaji P (2006) Bioconversion of lignocellulose materials. Mycobiology 34:159–165

    Google Scholar 

  3. 3.

    Sreenivasan E (2013) Bioconversion of industrial wood wastes into vermicompost by utilizing african night crawlers (Eudrilus eugeniae) Int J Adv Eng tech 19-20

  4. 4.

    Solá-Pérez JE, Saldarriaga-Noreña H, Murillo-Tovar M (2017) Ethyl levulinate obtained from lignocellulosic waste material with previous delignification by ultrasonic-assisted technique. J Agri Chem Env 6:93–103

    Google Scholar 

  5. 5.

    Giddel MR, Jivan AP (2007) Waste to wealth, potential of rice husk in India a literature review. International Conference on Cleaner Technologies and Environmental Management PEC, Pondicherry, India. January 4-6

  6. 6.

    Bayuaji R, Nuruddin MF (2014) Influence of microwave incinerated rice husk ash on hydration of foamed concrete. Adv Civ Eng 2014:1–8. https://doi.org/10.1155/2014/482176

    Article  Google Scholar 

  7. 7.

    Rao DK, Pranav PRT, Anusha M (2011) Stabilization of expansive soil with rice husk ash, lime and gypsum—an experimental study. Int J Eng Sci Technol 3:8076–8085

    Google Scholar 

  8. 8.

    Kumar A, Mohanta K, Kumar D, Parkash O (2012) Properties and industrial applications of rice husk: a review. Int J Emerging Technol Adv Eng 2:86–90

    Google Scholar 

  9. 9.

    Rozainee M, Ngo SP, Salema AA (2008) Effect of fluidizing velocity on the combustion of rice husk in a bench-scale fluidized bed combustor for the production of amorphous rice husk ash. Bioresour Technol 99:703–713

    Google Scholar 

  10. 10.

    Thongekkaew J, Patangtasa W, Jansri A (2014) Cellulase and xylanase production from Candida easanensis using agricultural wastes as a substrate. Songklan J Sci Technol 36:607–613

    Google Scholar 

  11. 11.

    Damiano VB, Bocchini DA, Gomes E, Da Silva R (2003) Application of crude xylanase from Bacillus licheniformis 77-2 to the bleaching of eucalyptus kraft pulp. World J Microbiol Biotechnol 19:139–144

    Google Scholar 

  12. 12.

    Ninawe S, Kuhad RC (2006) Bleaching of wheat straw-rich soda pulp with xylanase from a thermoalkalophilic Streptomyces cyaneus SN32. Bioresour Technol 97:2291–2295

    Google Scholar 

  13. 13.

    Ali UF, Saad El-Dein HS (2008) Production and partial purification of cellulase complex by Aspergillus niger and A. nidulans grown on water hyacinth blend. J Applied Sci Res 4:875–891

    Google Scholar 

  14. 14.

    Cobos A, Estrada P (2003) Effect of polyhydroxylic cosolvents on the thermostability and activity of xylanase from Trichoderma reesei QM 9414. Enzym Microb Technol 33:810–818

    Google Scholar 

  15. 15.

    Ryan SE, Nolan K, Thompson R, Gubitz GM, Savage AV, Tuohy MG (2003) Purification and characterization of a new low molecular weight endoxylanase from Penicillium capsulatum. Enz Microbial Technol 33:775–785

    Google Scholar 

  16. 16.

    Lu W, Li D, Wu Y (2003) Influence of water activity and temperature on xylanase biosynthesis in pilot-scale solid-state fermentation by Aspergillus sulphureus. Enz Microbial Technol 32:305–311

    Google Scholar 

  17. 17.

    Bayoumi RA, Yassin HM, Swelim MA, Abdel-All EZ (2008) Production of bacterial pectinase(s) from agro-industrial wastes under solid state fermentation conditions. J Applied Sci Res 4:1708–1721

    Google Scholar 

  18. 18.

    Fusawat P, Rakariyatham N (2014) Potential of cellulase and xylanase production by fungal strains using corn husks as substrate. Asia-Pacific J Sci Technol 19:229–234

    Google Scholar 

  19. 19.

    Adeleke MA, Akatah HA, Hassan AO, Adebimpe WO (2012) Microbial load and multiple drug resistance of pathogenic bacteria isolated from feaces and body surfaces of cockroaches in an urban area of southwestern Nigeria. The J Microbiol Biotechnol Food Sci 1(6):1448

    Google Scholar 

  20. 20.

    Smit E, Leeflang P, Glandorf B, van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Applied Env Microbiol 65:2614–2621

    Google Scholar 

  21. 21.

    Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Google Scholar 

  22. 22.

    Plackett RL, Burman JP (1946) The design of optimum multifactorial experiments. Biometrika 33:305–325

    MathSciNet  MATH  Google Scholar 

  23. 23.

    Box GE, Behnken DW (1960) Some new three level designs for the study of quantitative variables. Technometrics 2:455–475

    MathSciNet  Google Scholar 

  24. 24.

    Jung DU, Yoo HY, Kim SB, Lee JH, Park C, Kim SW (2015) Optimization of medium composition for enhanced cellulase production by mutant Penicillium brasilianum KUEB15 using statistical method. J Ind Eng Chem 25:145–150

    Google Scholar 

  25. 25.

    Draper NR (1963) “Ridge analysis” of response surfaces. Technometrics 5:469–479

    MATH  Google Scholar 

  26. 26.

    Myers RH (1976) Response surface methodology. Edwards Brothers, Ann Arbor, MI

    Google Scholar 

  27. 27.

    Khucharoenphaisan K, Tokuyama S, Kitpreechavanich V (2008) Statistical optimization of activity and stability of β-xylanase produced by newly isolated Thermomyces lanuginosus THKU-49 using central composite design. Afr J Biotechnol 7:3599–3602

    Google Scholar 

  28. 28.

    Trivedi S, Divecha J, Shah A (2012) Optimization of inulinase production by a newly isolated Aspergillus tubingensis CR16 using low cost substrates. Carb Polymers 90:483–490

    Google Scholar 

  29. 29.

    Embaby AM, Heshmat Y, Hussein A, Marey HS (2014) A sequential statistical approach towards an optimized production of a broad spectrum bacteriocin substance from a soil bacterium Bacillus sp. YAS 1 strain. The Sci World J. https://doi.org/10.1155/2014/396304

  30. 30.

    Embaby AM, Marey HS, Hussein A (2015) A statistical-mathematical model to optimize chicken feather waste bioconversion via Bacillus licheniformis SHG10: a low cost effective and ecologically safe approach. J Bioprocess Biotech 5:1

    Google Scholar 

  31. 31.

    Embaby AM, Melika RR, Hussein A, El-Kamel AH, Marey HS (2018) Biosynthesis of chitosan-oligosaccharides (COS) by non-aflatoxigenic Aspergillus sp. strain EGY1 DSM 101520: a robust biotechnological approach. Process Biochem 64:16–30

    Google Scholar 

  32. 32.

    Zambare V, Christopher L (2011) Statistical analysis of cellulase production in Bacillus amyloliquefaciens UNPDV-22. ELBA Bioflux 3:38–45

    Google Scholar 

  33. 33.

    Embaby AM, Hussein MN, Hussein A (2018) Monascus orange and red pigments production by Monascus purpureus ATCC16436 through co-solid state fermentation of corn cob and glycerol: an eco-friendly environmental low cost approach. PLoS One 13(12):e0207755. https://doi.org/10.1371/journal.pone.0207755

    Article  Google Scholar 

  34. 34.

    Anan A, Ghanem KM, Embaby AM, Hussein A, El-Naggar MY (2018) Statistically optimized ceftriaxone sodium biotransformation through Achrombacter xylosoxidans strain Cef6: unusual insight for bioremediation. J Basic Microbiol 58(2):120–130. https://doi.org/10.1002/jobm.201700497

    Article  Google Scholar 

  35. 35.

    Sonia KG, Chadha BS, Saini HS (2005) Sorghum straw for xylanase hyper-production by Thermomyces lanuginosus (D2W3) under solid-state fermentation. Bioresour Technol 96:1561–1569

    Google Scholar 

  36. 36.

    Chauhan P, Kumar G, Jain A (2013) Production of xylanases by Aspergillus terreus under liquid state fermentation conditions. Progress Agric 13:118–121

    Google Scholar 

  37. 37.

    Kumar KS, Manimaran A, Permaul K, Singh S (2009) Production of β-xylanase by a Thermomyces lanuginosus MC 134 mutant on corn cobs and its application in biobleaching of bagasse pulp. J Biosci Bioeng 107:494–498

    Google Scholar 

  38. 38.

    Gomes AFS, dos Santos BSL, Franciscon EG, Baffi MA (2016) Substrate and temperature effect on xylanase production by Aspergillus fumigatus using low cost agricultural wastes. Biosci J 32:915–921

    Google Scholar 

  39. 39.

    Krishna C (2005) Solid-state fermentation systems—an overview. Crit Rev Biotechnol 25:1–30

    Google Scholar 

  40. 40.

    Jain KK, Dey TB, Kumar S, Kuhad RC (2015) Production of thermostable hydrolases (cellulases and xylanase) from Thermoascus aurantiacus RCKK: a potential fungus. Bioprocess Biosyst Eng 38:787–796

    Google Scholar 

  41. 41.

    Gaffney M, Doyle S, Murphy R (2009) Optimization of xylanase production by Thermomyces lanuginosus in solid state fermentation. Biosci Biotechnol Biochem 73:2640–2644

    Google Scholar 

  42. 42.

    Mogk A, Mayer MP, Deuerling E (2002) Mechanisms of protein folding: molecular chaperones and their application in biotechnology. Chembiochem 3:807–814

    Google Scholar 

  43. 43.

    Jampala P, Tadikamalla S, Preethi M, Ramanujam S, Uppuluri KB (2017) Concurrent production of cellulase and xylanase from Trichoderma reesei NCIM 1186: enhancement of production by desirability-based multi-objective method. 3 Biotech. 7: 7-14

  44. 44.

    Jung DU, Yoo HY, Kim SB, Lee JH, Park C, Kim SW (2015) Optimization of medium composition for enhanced cellulase production by mutant Penicillium brasilianum KUEB15 using statistical method. J Ind Eng Chem 25:145–150

    Google Scholar 

  45. 45.

    Saha SP, Ghosh S (2014) Optimization of xylanase production by Penicillium citrinum xym2 and application in saccharification of agro-residues. Biocatal Agric Biotechnol 3:188–196

    Google Scholar 

  46. 46.

    Kachlishvili E, Penninckx MJ, Tsiklauri N, Elisashvili V (2006) Effect of nitrogen source on lignocellulolytic enzyme production by white-rot basidiomycetes under solid-state cultivation. World J Microbiol Biotechnol 22:391–397

    Google Scholar 

  47. 47.

    Bagewadi ZK, Mulla SI, Shouche Y, Ninnekar HZ (2016) Xylanase production from Penicillium citrinum isolate HZN13 using response surface methodology and characterization of immobilized xylanase on glutaraldehyde-activated calcium-alginate beads. 3 Biotech 6: 1-18

  48. 48.

    Senthilkumar SR, Ashokkumar B, Raj KC, Gunasekaran P (2005) Optimization of medium composition for alkali-stable xylanase production by Aspergillus fischeri Fxn 1 in solid-state fermentation using central composite rotary design. Bioresour Technol 96:1380–1386

    Google Scholar 

  49. 49.

    Gupta G, Sahai V, Gupta RK (2013) Optimization of xylanase production from Melanocarpus albomyces using wheat straw extract and its scale up in stirred tank bioreactor. Ind J Chem Technol 20:282–289

    Google Scholar 

  50. 50.

    Cui F, Zhao L (2012) Optimization of xylanase production from Penicillium sp. WX-Z1 by a two-step statistical strategy: Plackett-Burman and Box-Behnken experimental design. Int J Molecular Sci 13:10630–10646

    Google Scholar 

  51. 51.

    Ramanjaneyulu G, Reddy BR (2016) Optimization of xylanase production through response surface methodology by Fusarium sp. BVKT R2 isolated from forest soil and its application in saccharification. Front Microbiol 7:1–16

    Google Scholar 

  52. 52.

    Elisashvili V, Kachlishvili E, Penninckx M (2008) Effect of growth substrate, method of fermentation, and nitrogen source on lignocellulose-degrading enzymes production by white-rot basidiomycetes. J Ind Microbiol Miotechnol 35:1531–1538

    Google Scholar 

  53. 53.

    Bakri Y, Jacques P, Thonart P (2003) Xylanase production by Penicillium canescens 10–10c in solid-state fermentation. Appl Biochem Biotechnol 105-108:737–748

    Google Scholar 

  54. 54.

    Kar S, Mandal A, das Mohapatra PK, Mondal KC, Pati BR (2006) Production of cellulase-free xylanase by Trichoderma reesei SAF3. Braz J Biotechnol 37:462–464

    Google Scholar 

  55. 55.

    Torres JMO, TEE dC (2013) Production of xylanases by mangrove fungi from the Philippines and their application in enzymatic pretreatment of recycled paper pulps. World J Microbiol Biotechnol 29:645–655

    Google Scholar 

  56. 56.

    De Almeida MN, Guimarães VM, Falkoski DL, Paes GB et al (2014) Optimization of endoglucanase and xylanase activities from Fusarium verticillioides for simultaneous saccharification and fermentation of sugarcane bagasse. Appl Biochem Biotechnol 172:1332–1346

    Google Scholar 

  57. 57.

    Irfan M, Nadeem M, Syed Q (2014) One-factor-at-a-time (OFAT) optimization of xylanase production from Trichoderma viride-IR05 in solid-state fermentation. J Radiat Res Appl Sci 7:317–326

    Google Scholar 

  58. 58.

    Cunha L, Martarello R, PM dS, MM dF, KVG B, EXF F, Homem-de-Mello M, Magalhães PO (2018) Optimization of xylanase production from Aspergillus foetidus in soybean residue. Enz Res. https://doi.org/10.1155/2018/6597017

  59. 59.

    Ghosh VK, Deb JK (1988) Production and characterization of xylanase from Thielaviopsis basicola. Appl Microbiol Biotechnol 29:44–47

    Google Scholar 

  60. 60.

    Khalil AI, Krakowiak A, Russel S (2002) Production of extracellular cellulase and xylanase by the ligninolytic white-rot fungus Trametes versicolor grown on agricultural wastes. Ann Agric Sci 47:161–173

    Google Scholar 

  61. 61.

    Paterson RRM, Lima N (2017) Thermophilic fungi to dominate aflatoxigenic/mycotoxigenic fungi on food under global warming. Int J Environ Res Public Health 14:199. https://doi.org/10.3390/ijerph14020199

    Article  Google Scholar 

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AM: performed all laboratory work. AK: put the idea of the research, analyzed the data, and revised the manuscript draft. HM: performed the statistical modeling and its analysis. AE: participated in putting the research idea, wrote the whole manuscript, analyzed the data, and revised the draft manuscript.

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Correspondence to Amira M. Embaby.

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Matrawy, A.A., Khalil, A.I., Marey, H.S. et al. Biovalorization of the raw agro-industrial waste rice husk through directed production of xylanase by Thermomyces lanuginosus strain A3-1 DSM 105773: a statistical sequential model. Biomass Conv. Bioref. (2020). https://doi.org/10.1007/s13399-020-00824-9

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Keywords

  • Rice husk
  • Thermomyces lanuginosus A3-1 DSM 105773
  • Xylanase
  • Liquid-state fermentation
  • Eco-friendly low-cost approach