Skip to main content
SpringerLink
Log in

Statistical Optimization and Partial Characterization of Xylanases Produced by Streptomyces sp. S1M3I Using Olive Pomace as a Fermentation Substrate

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Xylanase production by Streptomyces sp. S1M3I was optimized by response surface methodology (RSM), followed by a partial characterization of these enzymes. Olive pomace was used as a substrate for growing Streptomyces sp. S1M3I in submerged fermentation. Effects of incubation time, pH, temperature, carbon source, nitrogen source, and inoculum size on xylanase production were studied, through the one-factor-at-a-time method. Then, a 33-factorial experimental design with RSM and the Box–Behnken design was investigated for the major influence factors. Maximum xylanase production (11.28 U/mL) was obtained when the strain was grown in mineral medium supplemented with 3% (w/v) of olive pomace powder and 0.3% (w/v) of ammonium sulfate, at a pH 7.4 and an incubation temperature of 40 °C. The xylanases in the supernatant degraded all tested substrates, with higher activity for the low-viscosity wheat arabinoxylan substrate. Two xylanases with close molecular masses were detected by zymogram analysis: Xyl-1 and Xyl-2 with molecular masses of 24.14 kDa and 27 kDa, respectively. The optimization of enzyme production parameters of Streptomyces sp. S1M3I and the characterization of these enzymes are prerequisites to enhancing xylanase production yield, which is crucial for further biotechnological processes.

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

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article.

References

  1. Thrash, J.C., & Coates, J.D. (2010). Phylum XVII, Acidobacteria phyl. nov. Bergey's Manual of Systematic Bacteriology. 725‑735. https://doi.org/10.1007/978-0-387-68572-4_6

  2. Boroujeni, M., Das, A., Prachanthi, K., et al. (2012). Enzymatic screening and rendom amplified polymorphic DNA fingerpinting of soil streptomycetes isolated from Wayanad District in Kerala. Indian Journal of Biological Sciences, 12, 1–8. https://doi.org/10.3923/jbs.2012.43.50

    Article  CAS  Google Scholar 

  3. Aparicio, J., Zoleica, M., Solá, S., Susana, C., et al. (2015). Safety versatility of Streptomyces sp. M7 to bioremediate soils co-contaminated with Cr (VI) and lindane. Ecotoxicology and Environmental Safety, 116, 34–39. https://doi.org/10.1016/j.ecoenv.2015.02.036

    Article  CAS  PubMed  Google Scholar 

  4. Prakash, D., Nawani, N., Prakash, M., et al. (2013). Actinomycetes : A repertory of green catalysts with a potential revenue resource. BioMed Research International, 2013, 1–8. https://doi.org/10.1155/2013/264020

    Article  CAS  Google Scholar 

  5. 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. Journal of Radiation Research and Applied Sciences, 7(3), 317–326. https://doi.org/10.1016/j.jrras.2014.04.004

    Article  Google Scholar 

  6. Garrido, M. M., Piccinni, F. E., Landoni, M., et al. (2022). Insights into the xylan degradation system of Cellulomonas sp. B6: biochemical characterization of rCsXyn10A and rCsAbf62A. Applied Microbiology and Biotechnology, 106(13), 5035–5049. https://doi.org/10.1007/S00253-022-12061-3

    Article  CAS  PubMed  Google Scholar 

  7. Gomathi, D., Muthulakshmi, C., Kumar, D. G., et al. (2012). Submerged fermentation of wheat bran by Aspergillus flavus for production and characterization of carboxy methyl cellulase. Asian Pacific Tropical Biomedical Magazine, 2(1), S67–S73. https://doi.org/10.1016/s2221-1691(12)60132-4

    Article  Google Scholar 

  8. Singhania, R. R., Sukumaran, R. K., Patel, A. K., et al. (2010). Advancement and comparative profiles in the production technologies using solid-state and submerged fermentation for microbial cellulases. Enzyme and Microbial Technology, 46(7), 541–549. https://doi.org/10.1016/j.enzmictec.2010.03.010

    Article  CAS  Google Scholar 

  9. Garai, D., & Kumar, V. (2013). Aqueous two phase extraction of alkaline fungal xylanase in PEG/phosphate system : Optimization by Box – Behnken design approach. Biocatalysis and Agricultural Biotechnology, 2(2), 125–131. https://doi.org/10.1016/j.bcab.2013.03.003

    Article  Google Scholar 

  10. Neifar, M., Jaouani, A., Ayari, A., et al. (2013). Improving the nutritive value of olive cake by solid state cultivation of the medicinal mushroom Fomes fomentarius. Chemosphere, 91, 110–114. https://doi.org/10.1016/j.chemosphere.2012.12.015

    Article  CAS  PubMed  Google Scholar 

  11. Macedo, E. P., Cerqueira, C. L. O., Souza, D. A. J., et al. (2013). Production of cellulose-degrading enzyme on sisal and other agro-industrial residues using a new Brazilian actinobacteria strain Streptomyces sp. SLBA-08. Brazilian Journal of Medical and Biological Research, 30(4), 729–735. https://doi.org/10.1590/s0104-66322013000400005

    Article  CAS  Google Scholar 

  12. Pagnanelli, F., Viggi, C. C., & Toro, L. (2010). Development of new composite biosorbents from olive pomace wastes. Applied Surface Science, 256(17), 5492–5497. https://doi.org/10.1016/j.apsusc.2009.12.146

    Article  CAS  Google Scholar 

  13. Leite, P., Manuel, J., Venâncio, A., et al. (2016). Ultrasounds pretreatment of olive pomace to improve xylanase and cellulase production by solid-state fermentation. Bioresource Technology, 214, 737–746. https://doi.org/10.1016/j.biortech.2016.05.028

    Article  CAS  PubMed  Google Scholar 

  14. Alam, Z., Muyibi, S. A., & Wahid, R. (2008). Statistical optimization of process conditions for cellulase production by liquid state bioconversion of domestic wastewater sludge. Bioresource Technology, 99, 4709–4716. https://doi.org/10.1016/j.biortech.2007.09.072

    Article  CAS  PubMed  Google Scholar 

  15. Karabegović, I. T., Stojičević, S. S., Veličković, D. T., et al. (2012). Optimization of microwave-assisted extraction of cherry laurel ( Prunus laurocerasus L.) fruit using response surface methodology. Engineering and Technology, 6, 897–902. https://doi.org/10.5281/zenodo.1085596

    Article  Google Scholar 

  16. Medouni-Haroune, L., Zaidi, F., Medouni-Adrar, S., et al. (2017) Selective isolation and screening of Actinobacteria strains producing lignocellulolytic enzymes using olive pomace as substrate. Iranian Journal of Biotechnology,15 (1), 74–77. https://doi.org/10.15171/ijb.1278.

  17. Medouni-Haroune, L., Zaidi, F., Medouni-Adrar, S., et al. (2017). Bioconversion of olive pomace by submerged cultivation of Streptomyces sp. S1M3I. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 88, 1425–1433. https://doi.org/10.1007/s40011-017-0880-x

    Article  CAS  Google Scholar 

  18. Lilitchan, S., Tangprawat, C., & Aryusuk, K. (2008). Partial extraction method for the rapid analysis of total lipids and c-oryzanol contents in rice bran. Food Chemistry, 106, 752–759. https://doi.org/10.1016/j.foodchem.2007.06.052

    Article  CAS  Google Scholar 

  19. Tuncer, M., Ball, A. S., Rob, A., et al. (1999). Optimization of extracellular lignocellulolytic enzyme production by a thermophilic actinomycete Thermomonospora fusca BD25. Enzyme and Microbial Technology, 25(1–2), 38–47. https://doi.org/10.1016/S0141-0229(99)00012-5

    Article  CAS  Google Scholar 

  20. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227(5259), 680–685. https://doi.org/10.1038/227680a0

  21. Dhillon, A., Gupta, J. K., & Khanna, S. (2000). Enhanced production, purification and characterisation of a novel cellulase-poor thermostable, alkalitolerant xylanase from Bacillus circulans AB 16. Process Biochemistry, 35, 849–856. https://doi.org/10.1016/s0032-9592(99)00152-1

    Article  CAS  Google Scholar 

  22. Danso, B., Ali, S. S., Xie, R., et al. (2022). Valorisation of wheat straw and bioethanol production by a novel xylanase and cellulase-producing Streptomyces strain isolated from the wood-feeding termite. Microcerotermes species. Fuel, 310, 122333. https://doi.org/10.1016/j.fuel.2021.122333

    Article  CAS  Google Scholar 

  23. Xiuting, L., Baoguo, S., Jin, Z., et al. (2011). Production and improved bleaching abilities of a thermostable xylanase from a newly isolated Streptomyces chartreusis strain. African Journal of Biotechnology, 10(64), 14132–14142. https://doi.org/10.5897/AJB10.2360

    Article  Google Scholar 

  24. Techapun, C., Charoenrat, T., Watanabe, M., et al. (2002). Optimization of thermostable and alkaline-tolerant cellulase-free xylanase production from agricultural waste by thermotolerant Streptomyces sp. Ab106, using the central composite experimental design. Biochemical Engineering Journal, 12, 99–105. https://doi.org/10.1016/s1369-703x(02)00047-5

    Article  CAS  Google Scholar 

  25. Khangkhachit, W., Suyotha, W., Leamdum, C., et al. (2021). Production of thermostable xylanase using Streptomyces thermocarboxydus ME742 and application in enzymatic conversion of xylan from oil palm empty fruit bunch to xylooligosaccharides. Biocatalysis and Agricultural Biotechnology, 37, 102180. https://doi.org/10.1016/j.bcab.2021.102180

    Article  CAS  Google Scholar 

  26. Romero, P., Lussier, M., Véronneau, S., et al. (1999). Mnt2p and Mnt3p of Saccharomyces cerevisiae are members of the Mnn1p family of alpha-1,3-mannosyltransferases responsible for adding the terminal mannose residues of O-linked oligosaccharides. Glycobiology, 9(10), 1045–1051. https://doi.org/10.1093/glycob/9.10.1045

    Article  CAS  PubMed  Google Scholar 

  27. Bajaj, B. K., & Singh, N. P. (2010). Production of xylanase from an alkali tolerant Streptomyces sp. 7b under solid-state fermentation, its purification, and characterization. Applied Biochemistry and Biotechnology, 162(6), 1804–1818. https://doi.org/10.1007/s12010-010-8960-x

    Article  CAS  PubMed  Google Scholar 

  28. Miyanaga, K., & Unno, H. (2011) Reaction kinetics, and stoichiometry. Comprehensive Biotechnology, 33–46. https://doi.org/10.1016/b978-0-08-088504-9.00085-4.

  29. Sharma, H. K., Xu, C., & Qin, W. (2021). Isolation of bacterial strain with xylanase and xylose/glucose isomerase (GI) activity and whole cell immobilization for improved enzyme production. Waste Biomass Valorization, 12, 833–845. https://doi.org/10.1007/s12649-020-01013-5

    Article  CAS  Google Scholar 

  30. Adhi, T. P., Korus, R. A., & Crawford, D. L. (1989). Production of major extracellular enzymes during lignocellulose degradation by two streptomycetes in agitated submerged culture. Applied and Environmental Microbiology, 55(5), 1165–1168. https://doi.org/10.1128/aem.55.5.1165-1168.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Boucherba, N., Benallaoua, S., Copinet, E., et al. (2011). Production and partial characterization of xylanase produced by Jonesia denitrificans isolated in Algerian soil. Process Biochemistry, 46(2), 519–525. https://doi.org/10.1016/j.procbio.2010.10.003

    Article  CAS  Google Scholar 

  32. McCarthy, A. (1987). Lignocellulose degrading actinomycetes. FEMS Microbiology Reviews, 46, 145–163.

    Article  CAS  Google Scholar 

  33. Vance, E. D., & Chapin, F. S. (2001). Substrate limitations to microbial activity in taiga forest floors. Soil Biology and Biochemistry, 33, 173–188.

    Article  CAS  Google Scholar 

  34. Naidu, G., & Panda, T. (1998). Production of pectolytic enzymes e a review. Bioprocess Engineering, 19, 355–361. https://doi.org/10.1007/pl00009023

    Article  CAS  Google Scholar 

  35. Salhi, M.O. (2004) Valorisation de sous-produits et déchets lignocellulosiques par culture de microorganismes cellulolytiques.Dissertation, Insitut national agronomique El-harrache.

  36. Kumar, A., Gupta, R., Shrivastava, B., et al. (2012). Xylanase production from an alkalophilic actinomycete isolate Streptomyces sp. RCK-2010, its characterization and application in saccharification of second generation biomass. Journal of Molecular Catalysis B: Enzymatic, 74(3–4), 170–177. https://doi.org/10.1016/j.molcatb.2011.10.001

    Article  CAS  Google Scholar 

  37. Nascimento, R. P., Coelho, R. R. R., Marques, S., et al. (2002). Production and partial characterisation of xylanase from Streptomyces sp. strain AMT-3 isolated from Brazilian cerrado soil. Enzyme and Microbial Technology, 31, 549–555. https://doi.org/10.1016/S0141-0229(02)00150-3

    Article  CAS  Google Scholar 

  38. Battestin, V., & Macedo, G. A. (2007). Effects of temperature, pH and additives on the activity of tannase produced by Paecilomyces variotii. Electronic Journal of Biotechnology, 10(2), 191–199. https://doi.org/10.2225/vol10-issue2-fulltext-9

    Article  CAS  Google Scholar 

  39. Haaland, P. D. (1989) Experimental design in biotechnology. New York.

  40. Sharma, P., & Bajaj, B. K. (2005). Production and partial characterization of alkali-tolerant xylanase from an alkalophilic Streptomyces sp. CD3. Journal of Scientific & Industrial Research, 64, 688–697.

    CAS  Google Scholar 

  41. Lafond, M., Tauzin, A., Desseaux, V., et al. (2011). GH10 xylanase D from Penicillium funiculosum : Biochemical studies and xylooligosaccharide production. Microbial Cell Factories, 10(1), 1–8. https://doi.org/10.1186/1475-2859-10-20

    Article  CAS  Google Scholar 

  42. Kulkarni, N., Shendye, A., & Rao, M. (1999). Molecular and biotechnological aspects of xylanases. FEMS Microbiology Reviews, 23(4), 411–456. https://doi.org/10.1111/j.1574-6976.1999.tb00407.x

    Article  CAS  PubMed  Google Scholar 

  43. Taibi, Z., Saoudi, B., Boudelaa, M., et al. (2012). Purification and biochemical characterization of a highly thermostable xylanase from Actinomadura sp. strain Cpt20 isolated from poultry compost. Applied Biochemistry and Biotechnology, 166, 663–679. https://doi.org/10.1007/s12010-011-9457-y

    Article  CAS  PubMed  Google Scholar 

  44. Chi, W., Park, D. Y., & Chang, Y. (2012). A novel alkaliphilic xylanase from the newly isolated mesophilic Bacillus sp. MX47: Production, purification and characterization. Applied Biochemistry and Biotechnology, 168, 899–909. https://doi.org/10.1007/s12010-012-9828-z

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Professor S. Roussos and V. Desseaux for the training in the IMBE and ISM2, Marseille (France).

Funding

The research was supported by the Faculty of Nature and Life Sciences, University of Bejaia, Algeria.

Author information

Authors and Affiliations

  1. Centre de Recherche en Technologies Agroalimentaires, Route de Targa Ouzemmour, Campus Universitaire, 06000, Bejaia, Algeria

    Lamia Medouni-Haroune, Cilia Bouiche & Khodir Madani

  2. Département Des Sciences Alimentaires, Faculté Des Sciences de La Nature Et de La Vie, Université de Bejaia, 06000, Bejaia, Algeria

    Sonia Medouni-Adrar

  3. Food, Nutrition and Health, Faculty of Land and Food Systems, The University of British Columbia, 2205 East Mall, Vancouver, BC, V6T 1Z4, Canada

    Aicha Asma Houfani

  4. Laboratoire de Microbiologie Appliquée, Faculté Des Sciences de La Nature Et de La Vie, Université de Bejaia, 06000, Bejaia, Algeria

    Zahra Azzouz & Mouloud Kecha

  5. Equipe Eco Technologies Et Bioremédiation, Faculté St Jérome, Campus Etoile, Aix Marseille Université & Université Avignon; IMBE UMR CNRS-7263/IRD-237, Case 421, 13397, Cedex 20, Marseille, France

    Sevastianos Roussos

  6. Institut Des Sciences Moléculaires de Marseille, Faculté Des Sciences Et Techniques, St Jérome, Biosciences UMR CNRS 6263.Université Paul Cézanne, 13397, Cedex 20, Marseille, France

    Véronique Desseaux

Authors
  1. Lamia Medouni-Haroune
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sonia Medouni-Adrar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aicha Asma Houfani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cilia Bouiche
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zahra Azzouz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sevastianos Roussos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Véronique Desseaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Khodir Madani
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mouloud Kecha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Lamia Medouni-Haroune: conceptualization, experiments, and writing original draft; Sonia Medouni-Adrar: methodology and data curation; Aicha Asma Houfani: reviewing and editing; Cilia Bouiche and Zahra Azzouz: polished the paper; Sevastianos Roussos: provides research guidance; Véronique Desseaux: analytical methodology; Khodir Madani and Mouloud Kecha: supervision. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lamia Medouni-Haroune.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Medouni-Haroune, L., Medouni-Adrar, S., Houfani, A.A. et al. Statistical Optimization and Partial Characterization of Xylanases Produced by Streptomyces sp. S1M3I Using Olive Pomace as a Fermentation Substrate. Appl Biochem Biotechnol 196, 2012–2030 (2024). https://doi.org/10.1007/s12010-023-04660-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-023-04660-1

Keywords

Search

Navigation