Skip to main content
SpringerLink
Log in

Isolation, screening wood rot fungi from the tropical forest of Thailand and their lignocellulolytic enzyme production under solid-state fermentation using agricultural waste as substrate

  • Original Article
  • Published:
Biomass Conversion and Biorefinery Aims and scope Submit manuscript

Abstract

The present study aimed to discover good lignocellulolytic enzyme (LCE) producers from Thailand’s tropical forest and then examine their multiple LCE production (including carboxymethyl cellulase (CMCase), xylanase, and laccase) using agricultural wastes as substrate. The total collection was 50 fungi, mainly from the Polyporales, Agaricales, and Xylariales orders. During primary screening by qualitative method and secondary screening by quantitative method, two potential fungi were proposed for multiple LCE production, including Auricularia auricula-judae 088 and Pseudolagarobasidium acaciicola TDW-48. Under solid-state fermentation (SSF) using agricultural wastes as substrates, P. acaciicola TDW-48 performed as a good producer that highly secreted simultaneous CMCase, xylanase, and laccase. In the next stage, the simplex lattice mixture design assessed the interaction of agricultural waste substrates and their effects on P. acaciicola TDW-48’s enzyme production. The results indicated that agricultural waste has different influences on CMCase, xylanase, and laccase production: orange peel showed a positive effect on both CMCase and xylanase activity, but a negative effect on laccase. In contrast, wheat bran positively influenced laccase, while it limited CMCase and xylanase. However, the combination of these substrates in the mixture showed synergic effects and improved enzyme activity. Through numerical optimization, a ternary mixture of wheat bran (1.27 g), orange peel (1.53 g), and rice husk (0.2 g) was identified as the most appropriate formulation for simultaneous multiple LCE production, reaching 20.96 U/g substrate for CMCase, 23.94 U/g substrate for xylanase, and 27.55 U/g substrate for laccase. These results provided a promising candidate for LCE production with high applicability in lignocellulose bioconversion and successfully demonstrated the relationship between the agricultural waste substrate and multiple LCE production that supported the enzyme production following the environmentally friendly and economical approach.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Data availability

The data supporting this study’s findings are available in the article.

References

  1. Chuen NL, Sabri M, Ghazali M et al (2021) Agro-waste-derived silica nanoparticles (Si-NPs) as biofertilizer. In: Bhat R (ed) Valorization of agri-food wastes and by-products. Academic Press, pp 881–897

    Chapter  Google Scholar 

  2. Liu Y, Tang Y, Gao H et al (2021) Challenges and future perspectives of promising biotechnologies for lignocellulosic biorefinery. Molecules 26:5411. https://doi.org/10.3390/molecules26175411

    Article  Google Scholar 

  3. Li H, Dou M, Wang X et al (2021) Optimization of cellulase production by a novel endophytic fungus Penicillium oxalicum R4 isolated from Taxus cuspidata. Sustainability 13:6006. https://doi.org/10.3390/su13116006

    Article  Google Scholar 

  4. Ubando AT, Felix CB, Chen W-H (2020) Review Biorefineries in circular bioeconomy: a comprehensive review. Bioresour Technol 299:122585. https://doi.org/10.1016/j.biortech.2019.122585

    Article  Google Scholar 

  5. Lopes AM, Ferreira Filho EX, Moreira LRS (2018) An update on enzymatic cocktails for lignocellulose breakdown. J Appl Microbiol 125:632–645. https://doi.org/10.1111/jam.13923

    Article  Google Scholar 

  6. Van Dyk JS, Pletschke BI (2012) A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes-factors affecting enzymes, conversion and synergy. Biotechnol Adv 30:1458–1480. https://doi.org/10.1016/j.biotechadv.2012.03.002

    Article  Google Scholar 

  7. Adsul M, Sandhu SK, Singhania RR et al (2020) Designing a cellulolytic enzyme cocktail for the efficient and economical conversion of lignocellulosic biomass to biofuels. Enzyme Microb Technol 133:109442. https://doi.org/10.1016/j.enzmictec.2019.109442

    Article  Google Scholar 

  8. Méndez-Líter JA, de Eugenio LI, Nieto-Domínguez M et al (2021) Hemicellulases from Penicillium and Talaromyces for lignocellulosic biomass valorization: a review. Bioresour Technol 324:124623. https://doi.org/10.1016/j.biortech.2020.124623

    Article  Google Scholar 

  9. Ma K, Ruan Z (2015) Production of a lignocellulolytic enzyme system for simultaneous bio-delignification and saccharification of corn stover employing co-culture of fungi. Bioresour Technol 175:586–593. https://doi.org/10.1016/j.biortech.2014.10.161

    Article  Google Scholar 

  10. Zhuo R, Fan F (2021) A comprehensive insight into the application of white rot fungi and their lignocellulolytic enzymes in the removal of organic pollutants. Sci Total Environ 778:146132. https://doi.org/10.1016/j.scitotenv.2021.146132

    Article  Google Scholar 

  11. Grelska A, Noszczyńska M (2020) White rot fungi can be a promising tool for removal of bisphenol A, bisphenol S, and nonylphenol from wastewater. Environ Sci Pollut Res Int 27:39958. https://doi.org/10.1007/S11356-020-10382-2

    Article  Google Scholar 

  12. Suryadi H, Judono JJ, Putri MR et al (2022) Biodelignification of lignocellulose using ligninolytic enzymes from white-rot fungi. Heliyon 8:e08865. https://doi.org/10.1016/j.heliyon.2022.e08865

    Article  Google Scholar 

  13. Santos FA, de Carvalho-Gonçalves LCT, de Carvalho Cardoso-Simões AL, de Melo Santos SF (2021) Evaluation of the production of cellulases by Penicillium sp. FSDE15 using corncob and wheat bran as substrates. Bioresour Technol Rep 14:100648. https://doi.org/10.1016/j.biteb.2021.100648

    Article  Google Scholar 

  14. Leite P, Sousa D, Fernandes H et al (2021) Recent advances in production of lignocellulolytic enzymes by solid-state fermentation of agro-industrial wastes. Curr Opin Green Sustain Chem 27:100407. https://doi.org/10.1016/j.cogsc.2020.100407

    Article  Google Scholar 

  15. Iram A, Cekmecelioglu D, Demirci A (2021) Ideal feedstock and fermentation process improvements for the production of lignocellulolytic enzymes. Processes 9:1–26. https://doi.org/10.3390/pr9010038

    Article  Google Scholar 

  16. Ohara A, Dos SJG, Angelotti JAF et al (2018) A multicomponent system based on a blend of agroindustrial wastes for the simultaneous production of industrially applicable enzymes by solid-state fermentation. Food Science and Technology (Brazil) 38:131–137. https://doi.org/10.1590/1678-457x.17017

    Article  Google Scholar 

  17. da Silva NN, Carneiro LL, de Menezes LHS et al (2020) Simplex-centroid design and artificial neural network-genetic algorithm for the optimization of exoglucanase production by Penicillium roqueforti ATCC 10110 through solid-state fermentation using a blend of agroindustrial wastes. Bioenergy Res 13:1130–1143. https://doi.org/10.1007/s12155-020-10157-0

    Article  Google Scholar 

  18. Ding S, Hu H, Gu JD (2020) Diversity, abundance, and distribution of wood-decay fungi in major parks of Hong Kong. Forests 11:1030. https://doi.org/10.3390/f11101030

    Article  Google Scholar 

  19. Senanayake IC, Rathnayaka AR, Marasinghe DS et al (2020) Morphological approaches in studying fungi: collection, examination, isolation, sporulation and preservation. Mycosphere 11:2678–2754. https://doi.org/10.5943/mycosphere/11/1/20

    Article  Google Scholar 

  20. Phillips R (2013) Mushrooms_ a comprehensive guide to mushroom identification. London, UK, Pan Macmillan

    Google Scholar 

  21. Barnett HL, Hunter BB (1998) Illustrated genera of imperfect fungi, fourth. Macmillan, New York

    Google Scholar 

  22. Guarro J, Gene J, Stchigel AM, Figueras MJ (2012) Atlas of soil Ascomycetes. In: CBS Biodiversity Series 10. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands

  23. Tangthirasunun N, Poeaim S (2022) Studies on the rapid and simple DNA extraction method, antibacterial activity and enzyme activity involved in plant biomass conversion by Cookeina sulcipes and C. tricholoma (cup fungi). J Pure Appl Microbiol 16:2851–2863. https://doi.org/10.22207/jpam.16.4.58

    Article  Google Scholar 

  24. Ghislain M, Zhang D, Herrera MR (1999) Molecular biology laboratory protocols: plant genotyping, 2nd edn. Crop Improvement and Genetic Resources Department, Training Manual, International Potato Center (CIP), Lima

  25. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, David H. Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, pp 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1

  26. Tangthirasunun N, Silar P, Bhat DJ et al (2014) Morphology and phylogeny of Pseudorobillarda eucalypti sp. nov., from Thailand. Phytotaxa 176:251–259. https://doi.org/10.11646/phytotaxa.176.1.24

    Article  Google Scholar 

  27. Neethu K, Rubeena M, Sajith S et al (2012) A novel strain of Trichoderma viride shows complete lignocellulolytic activities. Adv Biosci Biotechnol 03:1160–1166. https://doi.org/10.4236/abb.2012.38142

    Article  Google Scholar 

  28. Shrestha P, Joshi B, Joshi J et al (2016) Isolation and physicochemical characterization of laccase from Ganoderma lucidum-CDBT1 isolated from its native habitat in Nepal. Biomed Res Int 2016:3238909. https://doi.org/10.1155/2016/3238909

  29. Sánchez-Corzo LD, Álvarez-Gutiérrez PE, Meza-Gordillo R et al (2021) Lignocellulolytic enzyme production from wood rot fungi collected in Chiapas, Mexico, and their growth on lignocellulosic material. J Fungi 7:450. https://doi.org/10.3390/jof7060450

    Article  Google Scholar 

  30. Ghose TK (1987) Measurement of cellulase activities. Pure Appl Chem 59:257–268. https://doi.org/10.1351/pac198759020257

    Article  Google Scholar 

  31. Csarman F, Obermann T, Zanjko MC et al (2021) Functional expression and characterization of two laccases from the brown rot Fomitopsis pinicola. Enzyme Microb Technol 148:109801. https://doi.org/10.1016/j.enzmictec.2021.109801

    Article  Google Scholar 

  32. Cardoso WS, Queiroz PV, Tavares GP et al (2018) Multi-enzyme complex of white rot fungi in saccharification of lignocellulosic material. Braz J Microbiol 49:879–884. https://doi.org/10.1016/j.bjm.2018.05.006

    Article  Google Scholar 

  33. Berrin JG, Navarro D, Couturier M et al (2012) Exploring the natural fungal biodiversity of tropical and temperate forests toward improvement of biomass conversion. Appl Environ Microbiol 78:6483–6490. https://doi.org/10.1128/aem.01651-12

    Article  Google Scholar 

  34. Chew ALC, Desjardin DE, Tan Y-S et al (2015) Bioluminescent fungi from Peninsular Malaysia-a taxonomic and phylogenetic overview. Fungal Divers 70:149–187. https://doi.org/10.1007/s13225-014-0302-9

    Article  Google Scholar 

  35. Nguyen KA, Kumla J, Suwannarach N et al (2019) Optimization of high endoglucanase yields production from polypore fungus, Microporus xanthopus strain KA038 under solid-state fermentation using green tea waste. Biol Open 8:bio047183. https://doi.org/10.1242/bio.047183

    Article  Google Scholar 

  36. Metreveli E, Kachlishvili E, Singer SW, Elisashvili V (2017) Alteration of white-rot basidiomycetes cellulase and xylanase activities in the submerged co-cultivation and optimization of enzyme production by Irpex lacteus and Schizophyllum commune. Bioresour Technol 241:652–660. https://doi.org/10.1016/j.biortech.2017.05.148

    Article  Google Scholar 

  37. Vats A, Mishra S (2020) Laccase isoform diversity on basal medium in Cyathus bulleri and role in decolorization/detoxification of textile dyes and effluent. World J Microbiol Biotechnol 36:164. https://doi.org/10.1007/s11274-020-02939-7

    Article  Google Scholar 

  38. Adak A, Tiwari R, Singh S et al (2016) Laccase production by a novel white-rot fungus Pseudolagarobasidium acaciicola LA 1 through solid-state fermentation of Parthenium biomass and its application in dyes decolorization. Waste Biomass Valorization 7:1427–1435. https://doi.org/10.1007/s12649-016-9550-0

    Article  Google Scholar 

  39. Goh SM, Chan MY, Ong LGA (2017) Degradation potential of basidiomycetes Trametes ljubarskyi on Reactive Violet 5 (RV 5) using urea as optimum nitrogen source. Biotechnol Biotechnol Equip 31:743–748. https://doi.org/10.1080/13102818.2017.1334591

    Article  Google Scholar 

  40. Lu X, Li F, Zhou X et al (2022) Biomass, lignocellulolytic enzyme production and lignocellulose degradation patterns by Auricularia auricula during solid state fermentation of corn stalk residues under different pretreatments. Food Chem 384:132622. https://doi.org/10.1016/j.foodchem.2022.132622

  41. Coniglio RO, Fonseca MI, Villalba LL, Zapata PD (2017) Screening of new secretory cellulases from different supernatants of white rot fungi from Misiones, Argentina. Mycology 8:1–10. https://doi.org/10.1080/21501203.2016.1267047

    Article  Google Scholar 

  42. Pukahuta C, Suwanarit P, Shianagawa E et al (2004) Combination of laccase, xylanase and cellulase in lignocellulose degradation by white rot fungi, Lentinus polychrous Lev. and L. squarrosulus Mont. Kasetsart Journal - Natural Science 38:65–73

    Google Scholar 

  43. Vaithanomsat P, Sangnam A, Boonpratuang T et al (2013) Wood degradation and optimized laccase production by resupinate white-rot fungi in northern Thailand. Bioresources 8:6342–6360. https://doi.org/10.15376/biores.8.4.6342-6360

    Article  Google Scholar 

  44. Wang Q, Qian Y, Ma Y, Zhu C (2018) A preliminary study on the newly isolated high laccase-producing fungi: screening, strain characteristics and induction of laccase production. Open Life Sci 13:463–469. https://doi.org/10.1515/biol-2018-0055

    Article  Google Scholar 

  45. Thakur S, Gupte A (2015) Optimization and hyper production of laccase from novel agaricomycete Pseudolagarobasidium acaciicola AGST3 and its application in in vitro decolorization of dyes. Ann Microbiol 65:185–196. https://doi.org/10.1007/s13213-014-0849-4

    Article  Google Scholar 

  46. Teigiserova DA, Bourgine J, Thomsen M (2021) Closing the loop of cereal waste and residues with sustainable technologies: an overview of enzyme production via fungal solid-state fermentation. Sustain Prod Consum 27:845–857. https://doi.org/10.1016/j.spc.2021.02.010

    Article  Google Scholar 

  47. Xu X, Lin M, Zang Q, Shi S (2018) Solid state bioconversion of lignocellulosic residues by Inonotus obliquus for production of cellulolytic enzymes and saccharification. Bioresour Technol 247:88–95. https://doi.org/10.1016/j.biortech.2017.08.192

    Article  Google Scholar 

  48. Kaur J, Chugh P, Soni R, Soni SK (2020) A low-cost approach for the generation of enhanced sugars and ethanol from rice straw using in-house produced cellulase-hemicellulase consortium from A. niger P-19. Bioresour Technol Rep 11:100469. https://doi.org/10.1016/j.biteb.2020.100469

    Article  Google Scholar 

  49. Salomão GSB, Agnezi JC, Paulino LB et al (2019) Production of cellulases by solid state fermentation using natural and pretreated sugarcane bagasse with different fungi. Biocatal Agric Biotechnol 17:1–6. https://doi.org/10.1016/j.bcab.2018.10.019

    Article  Google Scholar 

  50. Sun HY, Li J, Zhao P, Peng M (2011) Banana peel: a novel substrate for cellulase production under solid-state fermentation. Afr J Biotechnol 10:17887–17890. https://doi.org/10.5897/ajb10.1825

    Article  Google Scholar 

  51. Atalla SMM, El Gamal NG (2020) Production and characterization of xylanase from pomegranate peel by Chaetomium globosum and its application on bean under greenhouse condition. Atalla Gamal Bull Nat Res Cent 44:104. https://doi.org/10.1186/s42269-020-00361-5

  52. Chakraborty S, Gupta R, Jain KK, Kuhad RC (2016) Cost-effective production of cellulose hydrolysing enzymes from Trichoderma sp. RCK65 under SSF and its evaluation in saccharification of cellulosic substrates. Bioprocess Biosyst Eng 39:1659–1670. https://doi.org/10.1007/s00449-016-1641-6

    Article  Google Scholar 

  53. da Silva DP, Pirota RDPB, Codima CA et al (2012) Using Amazon forest fungi and agricultural residues as a strategy to produce cellulolytic enzymes. Biomass Bioenergy 37:243–250. https://doi.org/10.1016/j.biombioe.2011.12.006

    Article  Google Scholar 

  54. Abd El Aty AA, Hamed ER, El-Beih AA, El-Diwany AI (2016) Induction and enhancement of the novel marine-derived Alternaria tenuissima KM651985 laccase enzyme using response surface methodology: application to Azo and Triphenylmethane dyes decolorization. J Appl Pharm Sci 6:6–14. https://doi.org/10.7324/japs.2016.60402

    Article  Google Scholar 

  55. Gautam A, Kumar A, Bharti AK, Dutt D (2018) Rice straw fermentation by Schizophyllum commune ARC-11 to produce high level of xylanase for its application in pre-bleaching. J Gen Eng Biotechnol 16:693–701. https://doi.org/10.1016/j.jgeb.2018.02.006

    Article  Google Scholar 

  56. Johnson Adeleke A, Olanbiwoninu A, Owoseni M et al (2012) Production of cellulase and pectinase from orange peels by fungi. Nat Sci (East Lansing) 10:107–112

    Google Scholar 

  57. Inácio FD, Ferreira RO, de Araujo CAV et al (2015) Production of enzymes and biotransformation of orange waste by Oyster mushroom, Pleurotus pulmonarius (Fr.) Quél. Adv Microbiol 05:1–8. https://doi.org/10.4236/aim.2015.51001

    Article  Google Scholar 

  58. Srivastava N, Srivastava M, Manikanta A et al (2017) Production and optimization of physicochemical parameters of cellulase using untreated orange waste by newly isolated Emericella variecolor NS3. Appl Biochem Biotechnol 183:601–612. https://doi.org/10.1007/s12010-017-2561-x

    Article  Google Scholar 

  59. Sharma D, Garlapati VK, Goel G (2016) Bioprocessing of wheat bran for the production of lignocellulolytic enzyme cocktail by Cotylidia pannosa under submerged conditions. Bioengineered 7:88–97. https://doi.org/10.1080/21655979.2016.1160190

    Article  Google Scholar 

  60. Taherzadeh-Ghahfarokhi M, Panahi R, Mokhtarani B (2019) Optimizing the combination of conventional carbonaceous additives of culture media to produce lignocellulose-degrading enzymes by Trichoderma reesei in solid state fermentation of agricultural residues. Renew Energy 131:946–955. https://doi.org/10.1016/j.renene.2018.07.130

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Assistant Professor Thanarak Chantaraprasit for helping to take good pictures during the sample collection. Thi Thu Huong Luong thanks King Mongkut’s Institute of Technology Ladkrabang for the doctoral scholarship.

Funding

This research was financially supported by King Mongkut’s Institute of Technology Ladkrabang (KMITL) under Grant numbers KDS2020/048 and A118-0261–010.

Author information

Authors and Affiliations

  1. Department of Biology, School of Science, King Mongkut’s Institute of Technology Ladkrabang (KMITL), Bangkok, Thailand

    Thi Thu Huong Luong, Supattra Poeaim & Narumon Tangthirasunun

  2. Laboratoire Interdisciplinaire Des Energies de Demain, Universite’ Paris Cite’, Paris, France

    Philippe Silar

Authors
  1. Thi Thu Huong Luong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philippe Silar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Supattra Poeaim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Narumon Tangthirasunun
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: TTHL and SP; writing—original draft preparation: TTHL; writing—review and editing: SP, PS, and TTHL; supervision: SP and NT. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Supattra Poeaim.

Ethics declarations

Ethical approval

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

Luong, T.T.H., Silar, P., Poeaim, S. et al. Isolation, screening wood rot fungi from the tropical forest of Thailand and their lignocellulolytic enzyme production under solid-state fermentation using agricultural waste as substrate. Biomass Conv. Bioref. (2023). https://doi.org/10.1007/s13399-023-05129-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13399-023-05129-1

Keywords

Search

Navigation