Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Upcycling the Spent Mushroom Substrate of the Grey Oyster Mushroom Pleurotus pulmonarius as a Source of Lignocellulolytic Enzymes for Palm Oil Mill Effluent Hydrolysis

  • Received : 2021.03.10
  • Accepted : 2021.04.27
  • Published : 2021.06.28
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Abstract

Mushroom cultivation along with the palm oil industry in Malaysia have contributed to large volumes of accumulated lignocellulosic residues that cause serious environmental pollution when these agroresidues are burned. In this study, we illustrated the utilization of lignocellulolytic enzymes from the spent mushroom substrate of Pleurotus pulmonarius for the hydrolysis of palm oil mill effluent (POME). The hydrolysate was used for the production of biohydrogen gas and enzyme assays were carried out to determine the productivities/activities of lignin peroxidase, laccase, xylanase, endoglucanase and β-glucosidase in spent mushroom substrate. Further, the enzyme cocktails were concentrated for the hydrolysis of POME. Central composite design of response surface methodology was performed to examine the effects of enzyme loading, incubation time and pH on the reducing sugar yield. Productivities of the enzymes for xylanase, laccase, endoglucanase, lignin peroxidase and β-glucosidase were 2.3, 4.1, 14.6, 214.1, and 915.4 U g-1, respectively. A maximum of 3.75 g/lof reducing sugar was obtained under optimized conditions of 15 h incubation time with 10% enzyme loading (v/v) at a pH of 4.8, which was consistent with the predicted reducing sugar concentration (3.76 g/l). The biohydrogen cumulative volume (302.78 ml H2.L-1 POME) and 83.52% biohydrogen gas were recorded using batch fermentation which indicated that the enzymes of spent mushroom substrate can be utilized for hydrolysis of POME.

Keywords

Acknowledgement

This research was funded by Postgraduate Research Fund, PPP under grant number PG064-2013B, University of Malaya, Malaysia and Ministry of Education Malaysia (MyBrainSc) Scholarship. The author would like to acknowledge Prof. Dr. Shaliza Ibrahim, Bidattul Syirat Zainal and Wan Nadzirah Meor Abdul Wahab for their contribution in this study.

References

  1. Massadeh MI, Modallal N. 2007. Ethanol production from olive mill wastewater (OMW) pretreated with Pleurotus sajor-caju. Energy Fuels 22: 150-154. https://doi.org/10.1021/ef7004145
  2. Singh AD, Vikineswary S, Abdullah N, Sekaran M. 2011. Enzymes from spent mushroom substrate of Pleurotus sajor-caju for the decolourisation and detoxification of textile dyes. World J. Microbiol. Biotechnol. 27: 535-545. https://doi.org/10.1007/s11274-010-0487-3
  3. Phan CW, Sabaratnam V. 2012. Potential uses of spent mushroom substrate and its associated lignocellulosic enzymes. Appl. Microbiol. Biotechnol. 96: 863-873. https://doi.org/10.1007/s00253-012-4446-9
  4. Khammuang S, Sarnthima R. 2007. Laccase from spent mushroom compost of Lentinus polychrous Lev. and its potential for remazol brilliant blue R decolorisation. Biotechnol. 6: 408-413. https://doi.org/10.3923/biotech.2007.408.413
  5. Finney KN, Ryu C, Sharifi VN, Swithenbank J. 2009. The reuse of spent mushroom compost and coal tailings for energy recovery: comparison of thermal treatment technologies. Bioresour. Technol. 100: 310-315. https://doi.org/10.1016/j.biortech.2008.05.054
  6. Shitole AV, Gade RM, Bandgar MS, Wavare SH, Belkar YK. 2014. Utilization of spent mushroom substrate as carrier for biocontrol agent and biofertilizer. Bioscan 9: 271-275.
  7. Zhu HJ, Sun LF, Zhang YF, Zhang XL, Qiao JJ. 2012. Conversion of spent mushroom substrate to biofertilizer using a stress-tolerant phosphate-solubilizing Pichia farinose FL7. Bioresour. Technol. 111: 410-416. https://doi.org/10.1016/j.biortech.2012.02.042
  8. Zhu HJ, Liu JH, Sun LF, Hu ZF, Qiao JJ. 2013. Combined alkali and acid pretreatment of spent mushroom substrate for reducing sugar and biofertilizer production. Bioresour. Technol. 136: 257-266. https://doi.org/10.1016/j.biortech.2013.02.121
  9. Wu S, Lan Y, Wu Z, Peng Y, Chen S, Huang Z, et al. 2013. Pretreatment of spent mushroom substrate for enhancing the conversion of fermentable sugar. Bioresour. Technol. 148: 596-600. https://doi.org/10.1016/j.biortech.2013.08.122
  10. Qiao JJ, Zhang YF, Sun LF, Liu WW, Zhu HJ, Zhang Z. 2011. Production of spent mushroom substrate hydrolysates useful for cultivation of Lactococcus lactis by dilute sulfuric acid, cellulase and xylanase treatment. Bioresour. Technol. 102: 8046-8051. https://doi.org/10.1016/j.biortech.2011.05.058
  11. Ko HG, Park SH, Ki S, Park HG, Park WM. 2005. Detection and recovery of hydrolytic enzymes from spent mushroom compost of four mushroom species. Folia Microbiol. 50: 103-106. https://doi.org/10.1007/BF02931456
  12. Schimpf U, Schulz R. 2016. Industrial by-products from white-rot fungi production. Part I: generation of enzyme preparations and chemical, protein biochemical and molecular biological characterization. Process Biochem. 51: 2034-2046. https://doi.org/10.1016/j.procbio.2016.08.032
  13. Ariff INM, Bahrin EK, Ramli N, Abd-Aziz S. 2017. Direct use of spent mushroom substrate from Pleurotus pulmonarius as a readily delignified feedstock for cellulase production. Waste Biomass Valori. 10: 839-850.
  14. Ismail I, Hassan MA, Rahman NAA, Soon CS. 2010. Thermophilic biohydrogen production from palm oil mill effluent (POME) using suspended mixed culture. Biomass Bioenerg. 34: 42-47. https://doi.org/10.1016/j.biombioe.2009.09.009
  15. Wu TY, Mohammad AW, Jahim JM, Anuar N. 2010. Pollution control technologies for the treatment of palm oil mill effluent (POME) through end-of-pipe processes. J. Environ. Manage 91: 1467-1490. https://doi.org/10.1016/j.jenvman.2010.02.008
  16. Silvamany H, Harun S, Mumtaz T, Jahim JM. 2015. Recovery of fermentable sugars from palm oil mill effluent via enzymatic hydrolysis. J. Teknol. 77: 115-121.
  17. Seong KT, Hassan MA, Ariff AB. 2008. Enzymatic saccharification of pretreated solid palm oil mill effluent and oil palm fruit fiber. Pertanika J. Sci. Technol. 16: 157-169.
  18. Khaw TS, Ariff AB. 2009. Optimization of enzymatic saccharification of palm oil mill effluent solid and oil palm fruit fibre to fermentable sugars. J. Trop Agric. Fd. Sci. 37: 85-94.
  19. Khaleb NA, Jahim JM, Kamal SA. 2012. Biohydrogen production using hydrolysates of palm oil mill effluent (POME). J. Asian Sci. Res. 2: 705-710.
  20. Sompong O, Prasertsan P, Karakashev D, Angelidaki I. 2008. Thermophilic fermentative hydrogen production by the newly isolated Thermoanaerobacterium thermosaccharolyticum PSU-2. Int. J. Hydrogen Energ. 33: 1204-1214. https://doi.org/10.1016/j.ijhydene.2007.12.015
  21. Mohammadi P, Ibrahim S, Annuar MSM. 2012. Effects of biomass, COD and bicarbonate concentrations on fermentative hydrogen production from POME by granulated sludge in a batch culture. Int. J. Hydrog. Energy 37: 17801-17808. https://doi.org/10.1016/j.ijhydene.2012.08.110
  22. Kamal SA, Jahim JM, Anuar N, Hassan O, Daud WRW, Mansor MF, et al. 2012. Pre-treatment effect of palm oil mill effluent (POME) during hydrogen production by a local isolate Clostridium butyricum. Int. J. Adv. Sci. Eng. Info. Technol. 2: 54-60.
  23. Mohammadi P, Ibrahim S, Mohamad Annuar MS. 2014. High-rate fermentative hydrogen production from palm oil mill effluent in an up-flow anaerobic sludge blanket-fixed film reactor. Chem. Eng. Res. Des. 92: 1811-1817. https://doi.org/10.1016/j.cherd.2014.04.023
  24. Krishnan S, Singh L, Sakinah M, Thakur S, Wahid ZA, Alkasrawi M. 2016. Process enhancement of hydrogen and methane production from palm oil mill effluent using two-stage thermophilic and mesophilic fermentation Int. J. Hydrog. Energy 41: 12888-12898. https://doi.org/10.1016/j.ijhydene.2016.05.037
  25. Zainal BS, Zinatizadeh AA, Chyuan OH, Mohd NS, Ibrahim S. 2017. Effects of process, operational and environmental variables on biohydrogen production using palm oil mill effluent (POME). Int. J. Hydrog. Energy 43: 10637-10644. https://doi.org/10.1016/j.ijhydene.2017.10.167
  26. Have RT, Hartmans S, Teunissen PJM, Field JA. 1998. Purification and characterization of two lignin peroxidase isozymes produced by Bjerkandera sp. strain BOS55. FEBS Lett. 422: 391-394. https://doi.org/10.1016/S0014-5793(98)00044-1
  27. Harkin JM, Obst JR. 1973. Syringaldazine, an effective reagent for detecting laccase and peroxidase in fungi. Experientia. 29: 381-387. https://doi.org/10.1007/BF01926734
  28. Leonowicz A, Grzywnowicz K. 1981. Quantitative estimation of laccase forms in some white-rot fungi using syringaldazine as a substrate. Enzyme Microb. Technol. 3: 55-58. https://doi.org/10.1016/0141-0229(81)90036-3
  29. Bailey MJ, Biely P, Poutanen K. 1992. Interlaboratory testing of methods for assay of xylanase activity. J. Biotechnol. 23: 257-270. https://doi.org/10.1016/0168-1656(92)90074-J
  30. Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31: 426-428. https://doi.org/10.1021/ac60147a030
  31. Kim DW, Kim TS, Jeong YK, Lee JK. 1992. Adsorption kinetics and behaviors of cellulase components on microcrystalline cellulose. J. Ferment. Bioeng. 73: 461-466. https://doi.org/10.1016/0922-338X(92)90138-K
  32. Zainal BS, Akhbari A, Zinatizadeh AA, Mohammadi P, Danaee M, Mohd NS, et al. 2019. UASFF start-up for biohydrogen and biomethane production from treatment of palm oil mill effluent. Int. J. Hydrog. Energy 44: 20725-20737. https://doi.org/10.1016/j.ijhydene.2018.07.037
  33. Choi J, Ahn Y. 2015. Biohydrogen fermentation from sucrose and piggery waste with high levels of bicarbonate alkalinity. Energies 8: 1716-1729. https://doi.org/10.3390/en8031716
  34. Cho NS, Malarczyk E, Nowak G, Nowak M, Kochmanska-Rdest J, Leonowicz A, et al. 2002. Changes in phenol oxidases and superoxide dismutase during fruit-body formation of Pleurotus on sawdust culture. Mycoscience 43: 267-270. https://doi.org/10.1007/S102670200039
  35. Montoya S, Orrego CE, Levin L. 2012. Growth, fruiting and lignocellulolytic enzyme production by the edible mushroom Grifola frondosa (maitake). World J. Microbiol. Biotechnol. 28: 1533-1541. https://doi.org/10.1007/s11274-011-0957-2
  36. Singh AD, Abdullah N, Vikineswary S. 2003. Optimization of extraction of bulk enzymes from spent mushroom compost. J. Chem. Technol. Biotechnol. 78: 743-752. https://doi.org/10.1002/jctb.852
  37. Binod P, Janu KU, Sindhu R, Pandey A. 2011. Hydrolysis of lignocellulosic biomass for bioethanol production. Biofuels, pp. 229-250. Elsevier Inc, Academic Press.
  38. Hiyama R, Gisusi S, Harada A. 2013. Effect of increased harvests on saccharification ratio of waste mushroom medium from the cultivation of shiitake mushroom (Lentinula edodes). J. Wood Sci. 59: 88-93. https://doi.org/10.1007/s10086-012-1293-3
  39. Eksioglu SD, Acharya A, Leightley LE, Arora S. 2009. Analyzing the design and management of biomass-to-biorefinery supply chain. Comput. Ind. Eng. 57: 1342-1352. https://doi.org/10.1016/j.cie.2009.07.003
  40. Zacchi G, Skoong K. Hahn-Hagerdal B. 1988. Economic evaluation of enzymatic hydrolysis of phenol-pretreated wheat straw. Biotechnol. Bioeng. 32: 460-468. https://doi.org/10.1002/bit.260320408
  41. Xu ZH, Bai YL, Xu X, Shi JS, Tao WY. 2005. Production of alkali-tolerant cellulase-free xylanase by Pseudomonas sp. WLUN024 with wheat bran as the main substrate. World J. Microbiol. Biotechnol. 21: 575-581. https://doi.org/10.1007/s11274-004-3491-7
  42. Aziz NIHA, Hanafiah MM. 2017. The potential of palm oil mill effluent (POME) as a renewable energy source. Acta Scientifica Malaysia 1: 9-11. https://doi.org/10.26480/asm.02.2017.09.11
  43. Wu TY, Mohammad AW, Jahim JM, Anuar N. 2009. A holistic approach to managing palm oil mill effluent (POME): biotechnological advances in the sustainable reuse of POME. Biotechnol. Adv. 27: 40-52. https://doi.org/10.1016/j.biotechadv.2008.08.005
  44. Yunus N, Jahim JM, Anuar N, Abdullah SRS, Kofli NT. 2014. Batch fermentative hydrogen production utilizing sago (Metroxylon sp.) starch processing effluent by enriched sago sludge consortia. Int. J. Hydrog. Energy 39: 19937-19946. https://doi.org/10.1016/j.ijhydene.2014.10.015
  45. Tarley CRT, Silveira G, dos Santos WNL, Matos GD, da Silva EGP, Bezerra MA, et al. 2009. Chemometric tools in electroanalytical chemistry: methods for optimization based on factorial design and response surface methodology. Microchem. J. 92: 58-67. https://doi.org/10.1016/j.microc.2009.02.002
  46. Neoh CH, Yahya A, Adnan R, Majid ZA, Ibrahim Z. 2013. Optimization of decolorization of palm oil mill effluent (POME) by growing cultures of Aspergillus fumigatus using response surface methodology. Environ. Sci. Pollut. R. 20: 2912-2923. https://doi.org/10.1007/s11356-012-1193-5
  47. Ladeira Azar RI, Bordignon-Junior SE, Laufer C, Specht J, Ferrier D, Kim D. 2020. Effect of lignin content on cellulolytic saccharification of liquid hot water pretreated sugarcane bagasse. Molecules 25: 623. https://doi.org/10.3390/molecules25030623
  48. Zhu L, O'Dwyer JP, Chang VS, Granda CB, Holtzapple MT. 2008. Structural features affecting biomass enzymatic digestibility. Bioresour. Technol. 99: 3817-3828. https://doi.org/10.1016/j.biortech.2007.07.033
  49. Mun WK, Rahman NA, Abd-Aziz S, Sabaratnam V, Hassan MA. 2008. Enzymatic hydrolysis of palm oil mill effluent solid using mixed cellulases from locally isolated fungi. Res. J. Microbiol. 3: 474-481. https://doi.org/10.3923/jm.2008.474.481
  50. Qiao JJ, Zhang YF, Sun LF, Liu WW, Zhu HJ, Zhang Z. 2011. Production of spent mushroom substrate hydrolysates useful for cultivation of Lactococcus lactis by dilute sulfuric acid, cellulase and xylanase treatment. Bioresour. Technol. 102: 8046-8051. https://doi.org/10.1016/j.biortech.2011.05.058
  51. Pandiyan K, Tiwari R, Singh S, Nain PKS, Rana S, Arora A, et al. 2014. Optimization of enzymatic saccharification of alkali pretreated Parthenium sp. using response surface methodology. Enzyme Res. 2014: 764898. https://doi.org/10.1155/2014/764898
  52. Ang SK, Adibah Y, Abd-aziz S, Madihah MS. 2015. Potential uses of xylanase-rich lignocellulolytic enzymes cocktail for oil palm trunk (OPT) degradation and lignocellulosic ethanol production. Energy Fuel. 29: 5103-5116. https://doi.org/10.1021/acs.energyfuels.5b00891
  53. Ferreira S, Duarte AP, Ribeiro MHL, Queiroz JA, Domingues FC. 2009. Response surface optimization of enzymatic hydrolysis of Cistus ladanifer and Cytisus striatus for bioethanol production. Biochem. Eng. J. 45: 192-200. https://doi.org/10.1016/j.bej.2009.03.012
  54. Gao Y, Xu J, Yuan Z, Zhang Y, Liu Y, Liang C. 2014. Optimization of fed-batch enzymatic hydrolysis from alkali-pretreated sugarcane bagasse for high-concentration sugar production. Bioresour Technol. 167: 41-45. https://doi.org/10.1016/j.biortech.2014.05.034
  55. Fang HHP, Liu H (2002) Effect of pH on hydrogen production from glucose by a mixed culture. Bioresour. Technol. 82: 87-93. https://doi.org/10.1016/S0960-8524(01)00110-9
  56. Norfadilah N, Raheem A, Harun R, Ahmadun FR. 2016. Bio-hydrogen production from palm oil mill effluent (POME): a preliminary study. Int. J. Hydrog. Energy 41: 11960-11964. https://doi.org/10.1016/j.ijhydene.2016.04.096
  57. Panagiotopoulos I, Bakker R, De Vrije T, Van Niel E, Koukios E, Claassen E. 2011. Exploring critical factors for fermentative hydrogen production from various type of lignocellulosic biomass. J. Jap. Inst. Energy 90: 363-368. https://doi.org/10.3775/jie.90.363
  58. Garritano AD, de Sa LRV, Aguieiras ECG, Freire DMG, Ferreira-Leitao VS. 2017. Efficient biohydrogen production via dark fermentation from hydrolized palm oil mill effluent by non-commercial enzyme preparation. Int. J. Hydrog. Energy 4249: 29166-29174.
  59. Chong ML, Rahim RA, Shirai Y, Hassan MA. 2009. Biohydrogen production by Clostridium butyricum EB6 from palm oil mill effluent. Int. J. Hydrog. Energy 34: 764-771. https://doi.org/10.1016/j.ijhydene.2008.10.095
  60. Zahrim AY, Rachel FM, Menaka S, Su SY, Melvin F, Chan ES. 2009. Decolourisation of anaerobic palm oil mill effluent via activated sludge-granular activated carbon. World Appl. Sci. J. 5: 126-129.
  61. Arooj MF, Han SK, Kim SH, Kim DH, Shin HS. 2008. Continuous biohydrogen production in a CSTR using starch as substrate. Int. J. Hydrog. Energy 33: 3289-3294. https://doi.org/10.1016/j.ijhydene.2008.04.022
  62. Cheng J, Su H, Zhou J, Song W, Cen, K. 2010. Microwave-assisted alkali pretreatment of rice straw to promote enzymatic hydrolysis and hydrogen production in dark- and photo-fermentation. Int. J. Hydrog. Energy 36: 2093 -2101. https://doi.org/10.1016/j.ijhydene.2010.11.021
  63. Ibrahim MF, Abd-Aziz S, Razak MNA, Phang LY, Hassan MA. 2012. Oil palm empty fruit bunch as alternative substrate for acetone -butanol -ethanol production by Clostridium butyricum EB6. Appl. Biochem. Biotechnol. 166: 1615-1625. https://doi.org/10.1007/s12010-012-9538-6
  64. Raghavi S, Sindhu R., Binod P, Gnansounou E, Pandey A. 2016. Development of a novel sequential pretreatment strategy for the production of bioethanol from sugarcane trash. Bioresour. Technol. 199: 202-210. https://doi.org/10.1016/j.biortech.2015.08.062
  65. Williams BC, McMullan JT, McCahey S. 2001. An initial assessment of spent mushroom compost as a potential energy feedstock. Bioresour. Technol. 79: 227-230. https://doi.org/10.1016/S0960-8524(01)00073-6
  66. Russel M, Basheer PAM, Rao JR. 2005. Potential use of spent mushroom compost ash as an activator for pulverized fuel ash. Constr. Build. Mater. 19: 698-702. https://doi.org/10.1016/j.conbuildmat.2005.02.020
  67. Hui Z, Jianhua L, Dai Jianqing CM, Yi C. 2007. The alternative uses of spent mushroom compost. Spore 4: 1-22.
  68. Najafi B, Faizollahzadeh AS, Shamshirband S, Chau KW. 2019. Spent mushroom compost (SMC) as a source for biogas production in Iran. Eng. Appl. Comput. Fluid Mech. 13: 967-982. https://doi.org/10.1080/19942060.2019.1658644

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