Abstract
The dephenolization of palm oil mill effluent (POME) with oil palm fiber-immobilized Trametes hirsuta AK 04 was conducted in a temporary immersion bioreactor to reduce the inhibitory effects of phenolics in anaerobic digestion. Longer immersion times provided greater removal of phenolics due to a higher release of manganese peroxidase. The most effective dephenolization was observed at 6 h immersed and 2 h non-immersed time (immersion ratio 6/8) with maximum removal of 85% from 1277 mg L−1 of phenolics in 4 days. The immobilized fungus maintained its high activity during multiple repeated batch treatments. The pretreated POME of 2 h showed higher methane yields compared with the untreated POME substrate. The methane yields increased with increasing pretreatment time and dephenolization levels. The results suggested that an increased abundance of methanogens was associated with the detoxification of phenolics. The fungal biomass contained crude protein, amino acids, and essential phenolics, which can be used as animal feed supplements.
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References
Akassou M, Kaanane A, Crolla A, Kinsley C (2010) Statistical modelling of the impact of some polyphenols on the efficiency of anaerobic digestion and the co-digestion of the wine distillery wastewater with dairy cattle manure and cheese whey. Water Sci Technol 62:475–483
APHA, AWWA, WEF (2012) Standard methods for the examination of water and wastewater, 22nd edn. American Public Health Association, Washington DC
Assas N, Ayed L, Marouani L, Hamdi M (2002) Decolorization of fresh and stored-black olive mill waste water by Geotrichum candidum. Process Biochem 38(3):361–365
Asses N, Ayed L, Bouallagui H, Sayadi S, Hamdi M (2009) Biodegradation of different molecular-mass polyphenols derived from olive mill wastewaters by Geotrichum candidum. Int Biodeterior Biodegradation 63:407–413
Banaszkiewicz T (2011) Nutritional value of soybean meal. In: El-Shemy H (ed) Soybean and nutrition, IntechOpen, pp 1-21
Bayburt C, Karaduman AB, Yenice Gürsu B, Tuncel M, Yamaç C (2019) Decolourization and detoxifcation of textile dyes by Lentinus arcularius in immersion bioreactor scale. Int J Environ Sci Technol 17:945–958
Boehmer U, Suhardi SH, Bley T (2006) Decolorizing reactive textile dyes with white-rot fungi by temporary immersion cultivation. Eng Life Sci 6(4):417–420
Chantho P, Musikavong C, Suttinun O (2016) Removal of phenolic compounds from palm oil mill effluent by thermophilic Bacillus thermoleovorans strain A2 and their effect on anaerobic digestion. Int Biodeterior Biodegradation 115:293–301
Cimmino R, Barone CMA, Claps S, Varricchio E, Rufrano D, Caroprese M, Albenzio M, Palo PD, Campanile G, Neglia G (2018) Effects of dietary supplementation with polyphenols on meat quality in Saanen goat kids. BMC Vet Res 14:181
Craig S, Helfrich LA (2009) Understanding fish nutrition, Feeds, and Feeding. Virginia Cooperative Extension:1–6
D’Annibale A, Crestini C, Vinciguerra V, Giovannozzi Sermanni G (1998) The biodegradation of recalcitrant effluents from an olive mill by a white-rot fungus. J Biotechnol 61:209–218
Dhouib A, Aloui F, Hamad N, Sayadi S (2006) Pilot-plant treatment of olive mill wastewaters by Phanerochaete chrysosporium coupled to anaerobic digestion and ultrafiltration. Process Biochem 41:159–167
Diamantopoulou P, Gardeli C, Papanikolaou S (2021) Impact of olive mill wastewaters on the physiological behavior of a wild-type new Ganoderma resinaceum isolate. Environ Sci Pollut Res 28:20570–20585
Dulf FV, Vodnar DC, Dulf EH, Pintea A (2017) Phenolic compounds, flavonoids, lipids and antioxidant potential of apricot (Prunus armeniaca L.) pomace fermented by two filamentous fungal strains in solid state system. Chem Cent J 11:92
Ergül FE, Sagin S, Öngen G, Sukan FV (2009) Dephenolisation of olive mill wastewater using adapted Trametes versicolor. Int Biodeterior Biodegradation 63:1–6
Field JA, Lenttiga G (1989) The effect of oxidative coloration on the methanogenic toxicity and anaerobic biodegradability of phenols. Biol Wastes 29(3):161–179
Freitas CS, Silva A, Perrone D, Vericimo MA, Baião DS, Pereira PR, Paschoain VMF, Aguila EMD (2019) Recovery of antimicrobials and bioaccessible isoflavones and phenolics from soybean (Glycine max) meal by aqueous extraction. Molecules 24:74
Folin O, Ciocalteu V (1927) On tyrosine and tryptophane determinations in proteins. J Biol Chem 73(2):627–650
Formolo M (2010) The microbial production of methane and other volatile hydrocarbons. In: Timmis KN (ed), Hanbook of hydrocarbon and lipid microbiology. Springer, Heidelberg, pp 113-126
Heinfling A, Martinez MJ, Martinez AT, Bergbaure M, Szewzyk U (1998) Transformation of industrial dyes by manganese peroxidase from Bjerkandera adusta and Pleurotus eryngii in a manganese-independent reaction. Appl Environ Microbiol 64(8):2788–2793
Hernandez JE, Edyvean RGJ (2008) Inhibition of biogas production and biodegradability by substituted phenolic compounds in anaerobic sludge. J Hazard Mater 160:20–28
Imami A, Riemer S, Schulze M, Amelung F, Gorshkov V, Rühl M, Ammenn J, Zorn H (2015) Depolymerization of lignosulfonates by submerged cultures of the basidiomycete Irpex consors and cloning of a putative versatile peroxidase. Enzym Microb Technol 81:8–15
Jamroz T, Sencio B, Gluszcz P, Ledakowicz S (2008) Effect of process conditions on the efficiency of laccase biosynthesis. Chem Process 29:293–303
Jaouani A, Tabka MG, Penninckx MJ (2006) Lignin modifying enzymes of Coriolosis polyzona and their role in olive mill wastewaters decolourisation. Chemosphere 62:1421–1430
Jarujareet P, Nakkanong K, Luepromchai E, Suttinun O (2019) Bioaugmentation coupled with phytoremediation for the removal of phenolic compounds and color from treated palm oil mill effluent. Environ Sci Pollut Res 26(31):32065–32079
Kaewmai R, H-Kittikun A, Suksaroj C, Musikavong C (2013) Alternative technologies for the reduction of greenhouse gas emissions from palm oil mills in Thailand. Environ Sci Technol 47:12417–12425
Kanwal HK, Reddy MS (2011) Effect of carbon, nitrogen sources and inducers on ligninolytic enzyme production by Morchella crassipes. World J Microbiol Biotechnol 27:687–691
Karimi S, Soofiani NM, Mahboubi A, Taherzadeh MJ (2018) Use of organic wastes and industrial by-products to produce filamentous fungi with potential as aqua-feed ingredients. Sustainability 10:3296
Kaufmann C, Sauer WC, Cervantes M, Zhang Y, He J, Rademacher M, Htoo JK (2005) Amino acid and energy digestibility in different sources of rice bran for growing pigs. Can J Anim Sci 85:355–363
Kietkwanboot A, Chaiprapat S, Müller R, Suttinun O (2020) Biodegradation of phenolic compounds present in palm oil mill effluent as single and mixed substrates by Trametes hirsuta AK04. J Environ Sci Health A 55(8):989–1002
Kietkwanboot A, Tran HTM, Suttinun O (2015) Simultaneous dephenolization and decolorization of treated palm oil mill effluent by oil palm fiber-immobilized Trametes Hirsuta strain AK 04. Water Air Soil Pollut 226:345
Kurbanoglu EB, Algur OF (2002) Single-cell protein production from ram horn hydrolysate by bacteria. Bioresour Technol 85(2):125–129
Li X, Rezaei R, Li P, Wu G (2011) Composition of amino acids in feed ingredients for animal diets. Amino Acids 40:1159–1168
Ma R, Yang R, Liu X, Chen Z, Yang C, Wang S (2015) Chemical composition and immunomodulatory activity of mycelia of the hairy bracket mushroom, Trametes hirsuta (higher basidiomycetes). Int J Med Mushrooms 17(3):267–276
Mustapha NA, Hu A, Yu CP, Sharuddin SS, Ramil N, Shirai Y, Maeda T (2018) Seeking key microorganisms for enhancing methane production in anaerobic digestion of waste sewage sludge. Appl Microbiol Biotechnol 102:5323–5334
Neoh CH, Lam CY, Lim CK, Yahya A, Ibrahim Z (2014) Decolorization of palm oil mill effluent using growing cultures of Curvularia clavata. Environ Sci Pollut Res 21:4397–4408
Nitayavardhana S, Issarapayup K, Pavasant P, Khanal SK (2013) Production of protein-rich fungal biomass in an airlift bioreactor using vinasse as substrate. Bioresour Technol 133:301–306
Nitayavardhana S, Khanal SK (2010) Innovative biorefinery concept for sugarbased ethanol industries: production of protein-rich fungal biomass on vinasse as an aquaculture feed ingredient. Bioresour Technol 101:9078–9085
Owen WF, Stuckey DC, Healy JB Jr, Young LY, McCarty PL (1979) Bioassay for monitoring biochemical methane potential and anaerobic toxicity. Water Res 13(6):485–492
Pandey A (1994) Solid-State Fermentation: an overview. In: Pandey A (ed) Solid state fermentation. Wiley, New Delhi, pp 3–10
Paramjeet S, Manasa P, Korrapati N (2018) Biofuels: Production of fungal-mediated ligninolytic enzymes and the modes of bioprocesses utilizing agro-based residues. Biocatal Agric Biotechnol 14:57–71
Peres MH, Oliva-Teles A (2009) The optimum dietary essential amino acid profile for gilthead seabream (Sparus aurata) juveniles. Aquaculture 296:81–86
Quek E, Ting YP, Tan HM (2006) Rhodococcus sp. F92 immobilized on polyurethane foam shows ability to degrade various petroleum products. Bioresour Technol 97:32–38
Rodrígues E, Pickard MA, Vazquez-Duhalt R (1999) Industrial dye decolorization by laccase from ligninolytic fungi. Curr Microbiol 38:27–32
Rodríguez Couto S (2011) Production of laccase and decolouration of the textile dye Remazol Brilliant Blue R in temporary immersion bioreactors. J Hazard Mater 194:297–302
Rodríguez Couto S, Sanroman MA, Hofer D, Gübitz GM (2004) Production of laccase by Trametes hirsuta grown in an immersion bioreactor and its application in the decolorisation of dyes from a leather factory. Eng Life Sci 4:233–237
Sankaran S, Khanal SK, Jasti N, Jin B, Pometto AL III, Leeuwen JHV (2010) Use of filamentous fungi for wastewater treatment and production of high value fungal byproducts: a review. Crit Rev Environ Sci Technol 40(5):400–449
Sar T, Ozturk M, Taherzadeh MJ, Ferreira JA (2020) New insights on protein recovery from olive oil mill wastewater through bioconversion with edible filamentous fungi. Processes 8:1210
Spiller M, Muys M, Papini G, Sakarika M, Buyle M, Vlaeminck SE (2020) Environmental impact of microbial protein from potato wastewater as feed ingredient: comparative consequential life cycle assessment of three production systems and soybean meal. Water Res 171:115406
Sun X, Bai R, Zhang Y, Wang Q, Fan X, Yuan J, Wang P (2013) Laccase-catalyzed oxidative polymerization of phenolic compounds. Biotechnol Appl Biochem 171:1673–1680
Usha KY, Praveen K, Reddy BR (2014) Enhanced production of ligninolytic enzymes by a mushroom Stereum ostrea. Biotechnol Res Int 2014:815495
Wanyo P, Meeso N, Siriamornpun S (2014) Effects of different treatments on the antioxidant properties and phenolic compounds of rice bran and rice husk. Food Chem 157:457–463
Yang S, Hai FI, Nghiem LD, Price WE, Roddick F, Moreira MT, Magram SF (2013) Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin modifying enzymes: a critical review. Bioresour Technol 141:97–108
Acknowledgements
The authors would like to thank the Agricultural Research Development Agency (Public Organization) and the Center of Excellence on Hazardous Substance Management (HSM) for their support in terms of facilities and scientific equipment.
Funding
This work was supported by the Thailand Research Fund and Taksin Palm (2521) Co., Ltd. through a Research and Researchers for Industries (RRI) Ph.D. Scholarship (Grant number PHD58I0021); and the graduate school dissertation fund, Prince of Songkla University, Thailand.
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AK conducted the experiment, processed the experimental data, contributed to the interpretation of the results, and drafted the manuscript. SC supervised the research, verified the analytical methods, and edited the manuscript. RM supervised the research and edited the manuscript. OS conceived and designed the study, supervised the findings of the study, verified the analytical methods, contributed to the interpretation of the results, acquired research funding, and was a major contributor in writing the manuscript. All authors read and approved the final manuscript.
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Kietkwanboot, A., Chaiprapat, S., Müller, R. et al. Dephenolization of palm oil mill effluent by oil palm fiber-immobilized Trametes hirsuta AK04 in temporary immersion bioreactor for the enhancement of biogas production. Environ Sci Pollut Res 29, 7559–7572 (2022). https://doi.org/10.1007/s11356-021-16199-x
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DOI: https://doi.org/10.1007/s11356-021-16199-x