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Production of laccase by repeated batch semi-solid fermentation using wheat straw as substrate and support for fungal growth

  • Antriksh Gupta
  • Asim Kumar Jana
Research Paper

Abstract

Repeated batch semi-solid fermentation (sSF) process using wheat straw substrate and fungal growth of Ganoderma lucidum on solid substrate was studied for production of laccase. pH showed significant effect on laccase production. Highest laccase activity with pH controlled to 5.0 in batch sSF was 15257.2 ± 353.4 U L− 1 on 9th day. In repeated batch process at pH 5.0, insoluble biomass substrate and fungal growth were reused after liquid part of medium was replaced with glucose, ammonium phosphate (best nitrogen source) and combined glucose and ammonium phosphate solution separately. Refilled to 80% w v− 1 of initial soluble sugar of first batch resulted in highest laccase production with peak activity after 4 days from replacement. Production of enzyme increased from 15257.2 U L− 1 in first batch to cumulative 90164.4 U L− 1 in 29 days after six repeated batches, productivity increased from 1680.2 to 3110.3 U L− 1 day− 1 (∼ 1.9 times) due to reductions in inhibitory effects and time required for fungal growth. Utilization of wheat straw in repeated batch sSF was supported by composition analysis and morphological changes (scanning electron microscopy) of substrate. Economic production of laccase using agricultural residues in repeated batch sSF could be possible.

Keywords

White rot fungi Semi-solid fermentation Repeated batch process Laccase production 

Notes

Acknowledgements

Mr Antriksh Gupta gratefully acknowledges Ministry of Human Resource Development (MHRD), Govt. of India, for providing the fellowship during the study. All authors are highly thankful to National Institute of Technology (NIT), Jalandhar, for providing grants and administrative supports for the study.

Compliance with ethical standards

Conflict of interest

Authors declare that they have no conflict of interest.

Supplementary material

449_2018_2053_MOESM1_ESM.pdf (173 kb)
Supplementary material 1 (PDF 173 KB)
449_2018_2053_MOESM2_ESM.pdf (114 kb)
Supplementary material 2 (PDF 113 KB)
449_2018_2053_MOESM3_ESM.pdf (100 kb)
Supplementary material 3 (PDF 99 KB)
449_2018_2053_MOESM4_ESM.pdf (10 kb)
Supplementary material 4 (PDF 10 KB)

References

  1. 1.
    Upadhyay P, Shrivastava R, Agrawal PK (2016) Bioprospecting and biotechnological applications of fungal laccase. 3 Biotech 6(1):15CrossRefGoogle Scholar
  2. 2.
    Hadibarata T, Syafiuddin A, Al-Dhabaan FA, Elshikh MS (2018) Biodegradation of Mordant orange-1 using newly isolated strain Trichoderma harzianum RY44 and its metabolite appraisal. Bioprocess Biosyst Eng 41(5):621–632CrossRefGoogle Scholar
  3. 3.
    Prakash H, Chauhan PS, General T, Sharma A (2018) Development of eco-friendly process for the production of bioethanol from banana peel using inhouse developed cocktail of thermo-alkali-stable depolymerizing enzymes. Bioprocess Biosyst Eng 41(7):1003–1016CrossRefGoogle Scholar
  4. 4.
    Zhuo R, Yuan P, Yang Y, Zhang S, Ma F, Zhang X (2017) Induction of laccase by metal ions and aromatic compounds in Pleurotus ostreatus HAUCC 162 and decolorization of different synthetic dyes by the extracellular laccase. Biochem Eng J 117:62–72CrossRefGoogle Scholar
  5. 5.
    Zeng S, Zhao J, Xia L (2017) Simultaneous production of laccase and degradation of bisphenol A with Trametes versicolor cultivated on agricultural wastes. Bioprocess Biosyst Eng 40(8):1237–1245CrossRefGoogle Scholar
  6. 6.
    Gonzalez JC, Medina SC, Rodriguez A, Osma JF, Alméciga-Díaz CJ, Sánchez OF (2013) Production of Trametes pubescens laccase under submerged and semi-solid culture conditions on agro-industrial wastes. PLoS One 8(9):e73721–e73735.  https://doi.org/10.1371/journal.pone.0073721 CrossRefGoogle Scholar
  7. 7.
    Parenti A, Muguerza E, Iroz AR, Omarini A, Conde E, Alfaro M, Castanera R, Santoyo F, Ramírez L, Pisabarro AG (2013) Induction of laccase activity in the white rot fungus Pleurotus ostreatus using water polluted with wheat straw extracts. Bioresour Technol 133:142–149.  https://doi.org/10.1016/j.biortech.2013.01.072 CrossRefGoogle Scholar
  8. 8.
    Tuor U, Winterhalter K, Fiechter a (1995) Enzymes of white-rot fungi involved in lignin degradation and ecological determinants for wood decay. J Biotechnol 41(1):1–17.  https://doi.org/10.1016/0168-1656(95)00042-O CrossRefGoogle Scholar
  9. 9.
    Hakala TK (2007) Characterization of the lignin-modifying enzymes of the selective white-rot fungus Physisporinus rivulosus, vol 1. Helsinki University Printing House, Helsinki, pp 1–60Google Scholar
  10. 10.
    Wang F, Hu J-H, Guo C, Liu C-Z (2014) Enhanced laccase production by Trametes versicolor using corn steep liquor as both nitrogen source and inducer. Bioresour Technol 166:602–605CrossRefGoogle Scholar
  11. 11.
    Wang H, Peng L, Ding Z, Wu J, Shi G (2015) Stimulated laccase production of Pleurotus ferulae JM301 fungus by Rhodotorula mucilaginosa yeast in co-culture. Process Biochem 50(6):901–905CrossRefGoogle Scholar
  12. 12.
    Zhu C, Bao G, Huang S (2016) Optimization of laccase production in the white-rot fungus Pleurotus ostreatus (ACCC 52857) induced through yeast extract and copper. Biotechnol Biotechnol Equip 30(2):270–276CrossRefGoogle Scholar
  13. 13.
    Birhanli E, Yesilada O (2010) Enhanced production of laccase in repeated-batch cultures of Funalia trogii and Trametes versicolor. Biochem Eng J 52(1):33–37CrossRefGoogle Scholar
  14. 14.
    Birhanli E, Erdogan S, Yesilada O, Onal Y (2013) Laccase production by newly isolated white rot fungus Funalia trogii: effect of immobilization matrix on laccase production. Biochem Eng J 71:134–139CrossRefGoogle Scholar
  15. 15.
    Singha S, Panda T (2014) Improved production of laccase by Daedalea flavida: consideration of evolutionary process optimization and batch-fed culture. Bioprocess Biosyst Eng 37(3):493–503CrossRefGoogle Scholar
  16. 16.
    Silvério SC, Moreira S, Milagres AM, Macedo EA, Teixeira JA, Mussatto SI (2013) Laccase production by free and immobilized mycelia of Peniophora cinerea and Trametes versicolor: a comparative study. Bioprocess Biosyst Eng 36(3):365–373CrossRefGoogle Scholar
  17. 17.
    Espinosa-Ortiz EJ, Rene ER, Pakshirajan K, van Hullebusch ED, Lens PN (2016) Fungal pelleted reactors in wastewater treatment: applications and perspectives. Chem Eng J 283:553–571CrossRefGoogle Scholar
  18. 18.
    Wan WAAQI, Ab Kadir S, Saari N (2016) The morphology of Ganoderma lucidum mycelium in a repeated-batch fermentation for exopolysaccharide production. Biotechnol Rep 11:2–11CrossRefGoogle Scholar
  19. 19.
    Adekunle AE, Zhang C, Guo C, Liu C-Z (2017) Laccase production from Trametes versicolor in solid-state fermentation of steam-exploded pretreated cornstalk. Waste Biomass Valoriz 8(1):153–159CrossRefGoogle Scholar
  20. 20.
    Wang Z, Liu J, Ning Y, Liao X, Jia Y (2017) Eichhornia crassipes: Agro-waster for a novel thermostable laccase production by Pycnoporus sanguineus SYBC-L1. J Biosci Bioeng 123(2):163–169CrossRefGoogle Scholar
  21. 21.
    Akpinar M, Urek RO (2017) Induction of fungal laccase production under solid state bioprocessing of new agroindustrial waste and its application on dye decolorization. 3 Biotech 7(2):98CrossRefGoogle Scholar
  22. 22.
    Machado I, Teixeira J, Rodríguez-Couto S (2013) Semi-solid-state fermentation: a promising alternative for neomycin production by the actinomycete Streptomyces fradiae. J Biotechnol 165(3–4):195–200.  https://doi.org/10.1016/j.jbiotec.2013.03.015 CrossRefGoogle Scholar
  23. 23.
    Osma JF, Moilanen U, Toca-Herrera JL, Rodríguez-Couto S (2011) Morphology and laccase production of white-rot fungi grown on wheat bran flakes under semi-solid-state fermentation conditions. FEMS Microbiol Lett 318(1):27–34.  https://doi.org/10.1111/j.1574-6968.2011.02234.x CrossRefGoogle Scholar
  24. 24.
    Barrios-González J (2012) Solid-state fermentation: physiology of solid medium, its molecular basis and applications. Process Biochem 47(2):175–185.  https://doi.org/10.1016/j.procbio.2011.11.016 CrossRefGoogle Scholar
  25. 25.
    Economou CN, Makri A, Aggelis G, Pavlou S, Vayenas DV (2010) Semi-solid state fermentation of sweet sorghum for the biotechnological production of single cell oil. Bioresour Technol 101(4):1385–1388.  https://doi.org/10.1016/j.biortech.2009.09.028 CrossRefGoogle Scholar
  26. 26.
    Gioia L, Manta C, Ovsejevi K, Menendez P, Rodriguez-couto S (2014) Enhancing laccase production by a newly-isolated strain of Pycnoporus sanguineus with high potential for dye decolouration. R Soc Chem Adv 4:34096–34103.  https://doi.org/10.1039/C4RA06039C CrossRefGoogle Scholar
  27. 27.
    Gupta A, Jana AK (2018) Effects of wheat straw solid contents in fermentation media on utilization of soluble/insoluble nutrient, fungal growth and laccase production. 3 Biotech 8(1):35.  https://doi.org/10.1007/s13205-017-1054-5 CrossRefGoogle Scholar
  28. 28.
    Mishra V, Jana AK (2017) Fungal pretreatment of sweet sorghum bagasse with combined CuSO4-gallic acid supplement for improvement in lignin degradation, selectivity, and enzymatic saccharification. Appl Biochem Biotechnol 183(1):200–217CrossRefGoogle Scholar
  29. 29.
    Pointing SB (1999) Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. Fungal Divers 2(3):17–33Google Scholar
  30. 30.
    Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 267(1):99–102CrossRefGoogle Scholar
  31. 31.
    Aidoo KE, Hendry R, Wood BJB (1981) Estimation of fungal growth in a solid-state fermentation system. Eur J Appl Microbiol Biotechnol 12(1):6–9CrossRefGoogle Scholar
  32. 32.
    Zhang J, Wang X-j, Wang J-p, Wang W-x (2014) Carbon and nitrogen contents in typical plants and soil profiles in Yanqi Basin of Northwest China. J Integr Agric 13(3):648–656CrossRefGoogle Scholar
  33. 33.
    Masson P, Dalix T, Bussière S (2010) Determination of major and trace elements in plant samples by inductively coupled plasma-mass spectrometry. Commun Soil Sci Plant Anal 41(3):231–243CrossRefGoogle Scholar
  34. 34.
    Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2010) Determination of structural carbohydrates and lignin in biomass: laboratory analytical procedure (LAP). National Renewable Energy Laboratory, GoldenGoogle Scholar
  35. 35.
    Arora DS, Chander M, Gill PK (2002) Involvement of lignin peroxidase, manganese peroxidase and laccase in degradation and selective ligninolysis of wheat straw. Int Biodeterior Biodegrad 50(2):115–120.  https://doi.org/10.1016/S0964-8305(02)00064-1 CrossRefGoogle Scholar
  36. 36.
    Kapich A, Prior B, Lundell T, Hatakka A (2005) A rapid method to quantify pro-oxidant activity in cultures of wood-decaying white-rot fungi. J Microbiol Methods 61(2):261–271CrossRefGoogle Scholar
  37. 37.
    Tinoco R, Acevedo A, Galindo E, Serrano-carreon L (2011) Increasing Pleurotus ostreatus laccase production by culture medium optimization and copper/lignin synergistic induction. J Ind Microbiol Biotechnol 38:531–540.  https://doi.org/10.1007/s10295-010-0797-3 CrossRefGoogle Scholar
  38. 38.
    Manavalan T, Manavalan A, Thangavelu KP, Heese K (2012) Secretome analysis of Ganoderma lucidum cultivated in sugarcane bagasse. J Proteom 77:298–309.  https://doi.org/10.1016/j.jprot.2012.09.004 CrossRefGoogle Scholar
  39. 39.
    Sitarz AK, Mikkelsen JD, Hojrup P, Meyer AS (2013) Identification of a laccase from Ganoderma lucidum CBS 229. 93 having potential for enhancing cellulase catalyzed lignocellulose degradation. Enzyme Microbial Technol 53(6–7):378–385.  https://doi.org/10.1016/j.enzmictec.2013.08.003 CrossRefGoogle Scholar
  40. 40.
    Jawson M, Elliott L (1986) Carbon and nitrogen transformations during wheat straw and root decomposition. Soil Biol Biochem 18(1):15–22CrossRefGoogle Scholar
  41. 41.
    Collins SR, Wellner N, Bordonado IM, Harper AL, Miller CN, Bancroft I, Waldron KW (2014) Variation in the chemical composition of wheat straw: the role of tissue ratio and composition. Biotechnol Biofuels 7(1):121CrossRefGoogle Scholar
  42. 42.
    Philippoussis A, Diamantopoulou P, Papadopoulou K, Lakhtar H, Roussos S, Parissopoulos G, Papanikolaou S (2010) Biomass, laccase and endoglucanase production by Lentinula edodes during solid state fermentation of reed grass, bean stalks and wheat straw residues. World J Microbiol Biotechnol 27(2):285–297.  https://doi.org/10.1007/s11274-010-0458-8 CrossRefGoogle Scholar
  43. 43.
    Shi J, Chinn MS, Sharma-Shivappa RR (2014) Interactions between fungal growth, substrate utilization, and enzyme production during solid substrate cultivation of Phanerochaete chrysosporium on cotton stalks. Bioprocess Biosyst Eng 37(12):2463–2473.  https://doi.org/10.1007/s00449-014-1224-3 CrossRefGoogle Scholar
  44. 44.
    Asgher M, Wahab A, Bilal M, Iqbal HMN (2016) Lignocellulose degradation and production of lignin modifying enzymes by Schizophyllum commune IBL-06 in solid-state fermentation. Biocatal Agric Biotechnol 6:195–201CrossRefGoogle Scholar
  45. 45.
    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 Biotechnol 35(11):1531–1538CrossRefGoogle Scholar
  46. 46.
    Plazonić I, Barbarić-Mikočević Ž, Antonović A (2016) Chemical composition of straw as an alternative material to wood raw material in fibre isolation. Drvna industrija: znanstveno-stručni časopis za pitanja drvne tehnologije 67(2):119CrossRefGoogle Scholar
  47. 47.
    Christensen BT, Bech-Andersen S (1989) Influence of straw disposal on distribution of amino acids in soil particle size fractions. Soil Biol Biochem 21(1):35–40CrossRefGoogle Scholar
  48. 48.
    Zhang A, Wang G, Gong G, Shen J (2017) Immobilization of white rot fungi to carbohydrate-rich corn cob as a basis for tertiary treatment of secondarily treated pulp and paper mill wastewater. Ind Crops Prod 109:538–541CrossRefGoogle Scholar
  49. 49.
    Zahmatkesh M, Spanjers H, van Lier JB (2018) A novel approach for application of white rot fungi in wastewater treatment under non-sterile conditions: immobilization of fungi on sorghum. Environ Technol 39(16):2030–2040CrossRefGoogle Scholar
  50. 50.
    Aydınoglu T, Sargın S (2013) Production of laccase from Trametes versicolor by solid-state fermentation using olive leaves as a phenolic substrate. Bioprocess Biosyst Eng 36(2):215–222CrossRefGoogle Scholar
  51. 51.
    Palmieri G, Bianco C, Cennamo G, Giardina P, Marino G, Monti M, Sannia G (2001) Purification, characterization, and functional role of a novel extracellular protease from Pleurotus ostreatus. Appl Environ Microbiol 67(6):2754–2759CrossRefGoogle Scholar
  52. 52.
    Abidi F, Limam F, Nejib MM (2008) Production of alkaline proteases by Botrytis cinerea using economic raw materials: assay as biodetergent. Process Biochem 43(11):1202–1208CrossRefGoogle Scholar
  53. 53.
    Meza JC, Auria R, Lomascolo A, Sigoillot J-C, Casalot L (2007) Role of ethanol on growth, laccase production and protease activity in Pycnoporus cinnabarinus ss3. Enzyme Microbial Technology 41(1):162–168CrossRefGoogle Scholar
  54. 54.
    Staszczak M, Zdunek E, Leonowicz A (2000) Studies on the role of proteases in the white-rot fungus Trametes versicolor: effect of PMSF and chloroquine on ligninolytic enzymes activity. J Basic Microbiol 40(1):51–63CrossRefGoogle Scholar
  55. 55.
    Chopra J, Sen R (2018) Process optimization involving critical evaluation of oxygen transfer, oxygen uptake and nitrogen limitation for enhanced biomass and lipid production by oleaginous yeast for biofuel application. Bioprocess Biosyst Eng 41(8):1103–1113CrossRefGoogle Scholar
  56. 56.
    Stajić M, Persky L, Friesem D, Hadar Y, Wasser SP, Nevo E, Vukojević J (2006) Effect of different carbon and nitrogen sources on laccase and peroxidases production by selected Pleurotus species. Enzyme Microbial Technol 38(1–2):65–73.  https://doi.org/10.1016/j.enzmictec.2005.03.026 CrossRefGoogle Scholar
  57. 57.
    Kenkebashvili N, Elisashvili V, Wasser SP (2012) Effect of carbon, nitrogen sources, and copper concentration on the ligninolytic enzyme production of Coriolopsis gallica. J Waste Convers Bioprod Biotechnol 1(2):22–27Google Scholar
  58. 58.
    Makela MR, Lundell T, Hatakka A, Hildén K (2013) Effect of copper, nutrient nitrogen, and wood-supplement on the production of lignin-modifying enzymes by the white-rot fungus Phlebia radiata. Fungal Biol 117(1):62–70CrossRefGoogle Scholar
  59. 59.
    Membrillo I, Sánchez C, Meneses M, Favela E, Loera O (2008) Effect of substrate particle size and additional nitrogen source on production of lignocellulolytic enzymes by Pleurotus ostreatus strains. Bioresour Technol 99(16):7842–7847CrossRefGoogle Scholar
  60. 60.
    Hailei W, Ping L, Yuhua Y, Yufeng L (2015) Overproduction of laccase from a newly isolated Ganoderma lucidum using the municipal food waste as main carbon and nitrogen supplement. Bioprocess Biosyst Eng 38(5):957–966CrossRefGoogle Scholar
  61. 61.
    Galhaup C, Wagner H, Hinterstoisser B, Haltrich D (2002) Increased production of laccase by the wood-degrading basidiomycete Trametes pubescens. Enzyme Microbial Technol 30(4):529–536CrossRefGoogle Scholar
  62. 62.
    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(4):391–397CrossRefGoogle Scholar
  63. 63.
    Couto SR, Gundín M, Lorenzo M, Sanromán M (2002) Screening of supports and inducers for laccase production by Trametes versicolor in semi-solid-state conditions. Process Biochem 38(2):249–255CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiotechnologyDr. B. R. Ambedkar National Institute of TechnologyJalandharIndia

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