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Applied Biochemistry and Biotechnology

, Volume 181, Issue 2, pp 844–859 | Cite as

Use of Swine Wastewater as Alternative Substrate for Mycelial Bioconversion of White Rot Fungi

  • Jangwoo Lee
  • Seung Gu Shin
  • Jinmo Ahn
  • Gyuseong Han
  • Kwanghyun Hwang
  • Woong Kim
  • Seokhwan HwangEmail author
Article

Abstract

Seven white rot fungal species were tested for growth as mycelia using swine wastewater (SW), an agro-waste with tremendous environmental footprint, as the sole nutrient source. The SW contained high concentrations of carbon and nitrogen components, which could support nutritional requirements for mycelial growth. Out of the seven species, Pleurotus ostreatus and Hericium erinaceus were successfully cultivated on the SW medium using solid-state fermentation. Response surface methodology was employed to determine the combination of pH, temperature (T), and substrate concentration (C) that maximizes mycelial growth rate (Kr) for the two species. The optimum condition was estimated as pH = 5.8, T = 28.8 °C, and C = 11.2 g chemical oxygen demand (COD)/L for P. ostreatus to yield Kr of 11.0 mm/day, whereas the greatest Kr (3.1 mm/day) was anticipated at pH = 4.6, T = 25.5 °C, and C = 11.9 g COD/L for H. erinaceus. These Kr values were comparable to growth rates obtained using other substrates in the literature. These results demonstrate that SW can be used as an effective substrate for mycelial cultivation of the two white rot fungal species, suggesting an alternative method to manage SW with the production of potentially valuable biomass.

Keywords

White rot fungi Mycelium Bioconversion Solid-state fermentation Optimization Response surface methodology 

Notes

Acknowledgments

This work was financially supported by Korea Ministry of Environment as “Knowledge based environmental service (Waste to energy recycling) Human resource development Project.” This work was also supported by “Human Resources Program in Energy Technology” of the Korea Institute of Energy Technology Evaluation and Planning (KETEP) Grant, funded by the Ministry of Trade, Industry and Energy, Republic of Korea (No. 20144030200460).

Supplementary material

12010_2016_2253_MOESM1_ESM.docx (236 kb)
Suppl. Fig. 1 (DOCX 236 kb)
12010_2016_2253_MOESM2_ESM.docx (19 kb)
Suppl. Fig. 2 (DOCX 18 kb)
12010_2016_2253_MOESM3_ESM.docx (19 kb)
Suppl. Fig. 3 (DOCX 18 kb)

References

  1. 1.
    APHA (2005). Standard methods for the examination of water and wastewater (21st ed.). Washington DC: American Public Health Association.Google Scholar
  2. 2.
    Bhak, G., Song, M., Lee, S., & Hwang, S. (2005). Response surface analysis of solid state growth of Pleurotus ostreatus mycelia utilizing whey permeate. Biotechnology Letters, 27, 1537–1541.CrossRefGoogle Scholar
  3. 3.
    Bhargav, S., Panda, B. P., Ali, M., & Javed, S. (2008). Solid-state fermentation: an overview. Chemical and Biochemical Engineering Quarterly, 22, 49–70.Google Scholar
  4. 4.
    Boddy, L., Crockatt, M. E., & Ainsworth, A. M. (2011). Ecology of Hericium cirrhatum, H. coralloides and H. erinaceus in the UK. Fungal Ecology, 4, 163–173.CrossRefGoogle Scholar
  5. 5.
    Boopathy, R. (1998). Biological treatment of swine waste using anaerobic baffled reactors. Bioresource Technology, 64, 1–6.CrossRefGoogle Scholar
  6. 6.
    Byler, D. M., & Susi, H. (1986). Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers, 25, 469–487.CrossRefGoogle Scholar
  7. 7.
    Cai, T., Park, S. Y., & Li, Y. (2013). Nutrient recovery from wastewater streams by microalgae: status and prospects. Renewable and Sustainable Energy Reviews, 19, 360–369.CrossRefGoogle Scholar
  8. 8.
    Canteri, H., & Ghoul, M. (2015). Submerged liquid culture for production of biomass and spores of Penicillium. Food Research International, 31, 262–278.CrossRefGoogle Scholar
  9. 9.
    Chen, Y., Cheng, J. J., & Creamer, K. S. (2008). Inhibition of anaerobic digestion process: a review. Bioresource Technology, 99, 4044–4064.CrossRefGoogle Scholar
  10. 10.
    Chen, Y., Huang, J., Li, Y., Zeng, G., Zhang, J., Huang, A., Zhang, J., Ma, S., Tan, X., Xu, W., & Zhou, W. (2015). Study of the rice straw biodegradation in mixed culture of Trichoderma viride and Aspergillus niger by GC-MS and FTIR. Environmental Science and Pollution Research, 22, 9807–9815.CrossRefGoogle Scholar
  11. 11.
    Cho, K., Lee, J., Han, G., Kim, N. K., Bae, H., & Hwang, S. (2015). Resource recovery using whey permeate to cultivate Phellinus linteus mycelium: solid-state and submerged liquid fermentation. Journal of Dairy Science, 98, 6739–6748.CrossRefGoogle Scholar
  12. 12.
    Cui, Y., Kim, D.-S., & Park, K.-C. (2005). Antioxidant effect of Inonotus obliquus. Journal of Ethnopharmacology, 96, 79–85.CrossRefGoogle Scholar
  13. 13.
    Dashtban, M., Schraft, H., Syed, T. A., & Qin, W. (2010). Fungal biodegradation and enzymatic modification of lignin. International Journal of Biochemistry and Molecular Biology, 1, 36–50.Google Scholar
  14. 14.
    DePasquale, D. A., & Montville, T. J. (1990). Mechanism by which ammonium bicarbonate and ammonium sulfate inhibit mycotoxigenic fungi. Applied and Environmental Microbiology, 56, 3711–3717.Google Scholar
  15. 15.
    El-Batal, A. I., ElKenawy, N. M., Yassin, A. S., & Amin, M. A. (2015). Laccase production by Pleurotus ostreatus and its application in synthesis of gold nanoparticles. Biotechnology Reports, 5, 31–39.CrossRefGoogle Scholar
  16. 16.
    Fan, L., Pandey, A., Mohan, R., & Soccol, C. (2000). Use of various coffee industry residues for the cultivation of Pleurotus ostreatus in solid state fermentation. Acta Biotechnologica, 20, 41–52.CrossRefGoogle Scholar
  17. 17.
    Fierer, N., Strickland, M. S., Liptzin, D., Bradford, M. A., & Cleveland, C. C. (2009). Global patterns in belowground communities. Ecology Letters, 12, 1238–1249.CrossRefGoogle Scholar
  18. 18.
    Figlas, D., Matute, R. G., & Curvetto, N. R. (2007). Cultivation of culinary-medicinal lion’s mane mushroom Hericium erinaceus (Bull.: Fr.) Pers. (Aphyllophoromycetideae) on substrate containing sunflower seed hulls. International Journal Medical Mushrooms, 9, 67–73.CrossRefGoogle Scholar
  19. 19.
    Hamilton, D., Luce, W. and Heald, A. (1997). Production and characteristics of swine manure. Stillwater, OK: Oklahoma Cooperative Extension Service.Google Scholar
  20. 20.
    Hendriks, A. T. W. M., & Zeeman, G. (2009). Pretreatments to enhance the digestibility of lignocellulosic biomass. Bioresource Technology, 100, 10–18.CrossRefGoogle Scholar
  21. 21.
    Hoa, H. T., & Wang, C.-L. (2015). The effects of temperature and nutritional conditions on mycelium growth of two oyster mushrooms (Pleurotus ostreatus and Pleurotus cystidiosus). Mycobiology, 43, 14–23.CrossRefGoogle Scholar
  22. 22.
    Huang, D., Cui, F., Li, Y., Zhang, Z., Zhao, J., Han, X., Xiao, X., Qian, J., Wu, Q., & Guan, G. (2007). Nutritional requirements for the mycelial biomass and exopolymer production by Hericium erinaceus CZ-2. Food Technology and Biotechnology, 45, 389–395.Google Scholar
  23. 23.
    Huang, L., Wen, X., Wang, Y., Zou, Y., Ma, B., Liao, X., Liang, J., & Wu, Y. (2014). Effect of the chlortetracycline addition method on methane production from the anaerobic digestion of swine wastewater. Journal of Environmental Sciences, 26, 2001–2006.CrossRefGoogle Scholar
  24. 24.
    Hwang, S., Lee, Y., & Yang, K. (2001). Maximization of acetic acid production in partial acidogenesis of swine wastewater. Biotechnology and Bioengineering, 75, 521–529.CrossRefGoogle Scholar
  25. 25.
    Ishikawa, K., Matsui, I., Honda, K., & Nakatani, H. (1990). Substrate-dependent shift of optimum pH in porcine pancreatic alpha-amylase-catalyzed reactions. Biochemistry, 29, 7119–7123.CrossRefGoogle Scholar
  26. 26.
    Klimek, B., Fyda, J., Pajdak-Stos, A., Kocerba, W., Fiakowska, E., & Sobczyk, M. (2012). Toxicity of ammonia nitrogen to ciliated protozoa Stentor coeruleus and Coleps hirtus isolated from activated sludge of wastewater treatment plants. B Environ Contam Tox, 89, 975–977.CrossRefGoogle Scholar
  27. 27.
    Lahav, O., Schwartz, Y., Nativ, P., & Gendel, Y. (2013). Sustainable removal of ammonia from anaerobic-lagoon swine waste effluents using an electrochemically-regenerated ion exchange process. Chemical Engineering Journal, 218, 214–222.CrossRefGoogle Scholar
  28. 28.
    Lee, C., Lee, S., Cho, K.-J., & Hwang, S. (2011a). Mycelial cultivation of Phellinus linteus using cheese-processing waste and optimization of bioconversion conditions. Biodegradation, 22, 103–110.CrossRefGoogle Scholar
  29. 29.
    Lee, H., Song, M., & Hwang, S. (2003). Optimizing bioconversion of deproteinated cheese whey to mycelia of Ganoderma lucidum. Process Biochemistry, 38, 1685–1693.CrossRefGoogle Scholar
  30. 30.
    Lee, J. (1997). Biological conversion of lignocellulosic biomass to ethanol. Journal of Biotechnology, 56, 1–24.CrossRefGoogle Scholar
  31. 31.
    Lee, S., Bae, H., Song, M., & Hwang, S. (2008). Bioconversion of starch processing waste to Phellinus linteus mycelium in solid-state cultivation. Journal of Industrial Microbiology & Biotechnology, 35, 859–865.CrossRefGoogle Scholar
  32. 32.
    Luo, L., He, H., Yang, C., Wen, S., Zeng, G., Wu, M., Zhou, Z., & Lou, W. (2016). Nutrient removal and lipid production by Coelastrella sp. in anaerobically and aerobically treated swine wastewater. Bioresource Technology, 216, 135–141.CrossRefGoogle Scholar
  33. 33.
    MacMillan, A. (1956). The entry of ammonia into fungal cells. Journal of Experimental Botany, 113–126.Google Scholar
  34. 34.
    Macris, B., & Markakis, P. (1981). Characterization of extracellular β-d-galactosidase from Fusarium moniliforme grown in whey. Applied and Environmental Microbiology, 41, 956–958.Google Scholar
  35. 35.
    Malinowska, E., Krzyczkowski, W., Lapienis, G., & Herold, F. (2009). Improved simultaneous production of mycelial biomass and polysaccharides by submerged culture of Hericium erinaceum: optimization using a central composite rotatable design (CCRD). Journal of Industrial Microbiology & Biotechnology, 36, 1513–1527.CrossRefGoogle Scholar
  36. 36.
    Mikeš, V., Zofall, M., Chytil, M., Fulneček, J., & Scháně, L. (1994). Ammonia-assimilating enzymes in the basidiomycete fungus Pleurotus ostreatus. Microbiology, 140, 977–982.CrossRefGoogle Scholar
  37. 37.
    Mishra, A., & Kumar, S. (2007). Cyanobacterial biomass as N-supplement to agro-waste for hyper-production of laccase from Pleurotus ostreatus in solid state fermentation. Process Biochemistry, 42, 681–685.CrossRefGoogle Scholar
  38. 38.
    MoE. (2012). Statistical data of Korean national livestock manure treatment (가축분뇨 처리 통계). In Environment, M. o. (ed). Korea Ministry of Environment: Sejong.Google Scholar
  39. 39.
    Muniraj, I. K., Xiao, L., Liu, H., & Zhan, X. (2015). Utilisation of potato processing wastewater for microbial lipids and γ-linolenic acid production by oleaginous fungi. Journal of the Science of Food and Agriculture, 95, 3084–3090.CrossRefGoogle Scholar
  40. 40.
    Palmieri, G., Cennamo, G., Faraco, V., Amoresano, A., Sannia, G., & Giardina, P. (2003). Atypical laccase isoenzymes from copper supplemented Pleurotus ostreatus cultures. Enzyme Microb Tech, 33, 220–230.CrossRefGoogle Scholar
  41. 41.
    Pandey, A. (2003). Solid-state fermentation. Biochemical Engineering Journal, 13, 81–84.CrossRefGoogle Scholar
  42. 42.
    Patrick, D., Fabien, V., Camille, B. and Fabrice, B. (2008). Microbiological aspects of methane production during pig manure storage. 13th International Conference of the FAO ESCORENA Network on Recycling of Agricultural, Municipal and Industrial Residues in Agriculture (pp. 96–99). Albena, Bulgaria.Google Scholar
  43. 43.
    Prasad, K. K., Mohan, S. V., Bhaskar, Y. V., Ramanaiah, S. V., Babu, V. L., Pati, B. R., & Sarma, P. N. (2005). Laccase production using Pleurotus ostreatus 1804 immobilized on PUF cubes in batch and packed bed reactors: influence of culture conditions. Journal of Microbiology, 43, 301–307.Google Scholar
  44. 44.
    Rahardjo, Y. S. P., Tramper, J., & Rinzema, A. (2006). Modeling conversion and transport phenomena in solid-state fermentation: a review and perspectives. Biotechnology Advances, 24, 161–179.CrossRefGoogle Scholar
  45. 45.
    Rousk, J., & Bååth, E. (2007). Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiology Ecology, 62, 258–267.CrossRefGoogle Scholar
  46. 46.
    Royse, D. J. (2014). A global perspective on the high five: Agaricus, Pleurotus, Lentinula, Auricularia & Flammulina. Proceedings of the 8th International Conference on Mushroom Biology and Mushroom Products (ICMBMP8) (pp. 1–6).Google Scholar
  47. 47.
    Rudolfová, J., & Mikeš, V. (1997). Involvement of the glutamine synthetase/glutamate synthase pathway in ammonia assimilation by the wood-rotting fungus Pleurotus ostreatus. Folia Microbiologica, 42, 577–582.CrossRefGoogle Scholar
  48. 48.
    Sánchez, C. (2009). Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnology Advances, 27, 185–194.CrossRefGoogle Scholar
  49. 49.
    Sánchez, C. (2010). Cultivation of Pleurotus ostreatus and other edible mushrooms. Applied Microbiology and Biotechnology, 85, 1321–1337.CrossRefGoogle Scholar
  50. 50.
    Sang, B.-I., Hori, K., Tanji, Y., & Unno, H. (2001). A kinetic analysis of the fungal degradation process of poly (3-hydroxybutyrate-co-3-hydroxyvalerate) in soil. Biochemical Engineering Journal, 9, 175–184.CrossRefGoogle Scholar
  51. 51.
    Sharma, S., Verma, M., & Sharma, A. (2013). Utilization of non edible oil seed cakes as substrate for growth of Paecilomyces lilacinus and as biopesticide against termites. Waste and Biomass Valorization, 4, 325–330.CrossRefGoogle Scholar
  52. 52.
    Smidt, E., & Schwanninger, M. (2005). Characterization of waste materials using FTIR spectroscopy: process monitoring and quality assessment. Spectroscopy Letters, 38, 247–270.CrossRefGoogle Scholar
  53. 53.
    Song, M., Kim, N., Lee, S., & Hwang, S. (2007). Use of whey permeate for cultivating Ganoderma lucidum mycelia. Journal of Dairy Science, 90, 2141–2146.CrossRefGoogle Scholar
  54. 54.
    Suguimoto, H. H., Barbosa, A. M., Dekker, R. F., & Castro-Gomez, R. J. (2001). Veratryl alcohol stimulates fruiting body formation in the oyster mushroom, Pleurotus ostreatus. FEMS Microbiology Letters, 194, 235–238.CrossRefGoogle Scholar
  55. 55.
    Sun, Y., & Cheng, J. Y. (2002). Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresource Technology, 83, 1–11.CrossRefGoogle Scholar
  56. 56.
    Tice, R. C., & Kim, Y. (2014). Influence of substrate concentration and feed frequency on ammonia inhibition in microbial fuel cells. Journal of Power Sources, 271, 360–365.CrossRefGoogle Scholar
  57. 57.
    Tuesorn, S., Wongwilaiwalin, S., Champreda, V., Leethochawalit, M., Nopharatana, A., Techkarnjanaruk, S., & Chaiprasert, P. (2013). Enhancement of biogas production from swine manure by a lignocellulolytic microbial consortium. Bioresource Technology, 144, 579–586.CrossRefGoogle Scholar
  58. 58.
    USDA. (2015). Livestock and poultry: world markets and trade. In Agriculture, U. S. D. o. (Ed). Wasington DC: United States Department of Agriculture.Google Scholar
  59. 59.
    Van Dyk, J. S., & Pletschke, B. I. (2012). A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes—factors affecting enzymes, conversion and synergy. Biotechnology Advances, 30, 1458–1480.CrossRefGoogle Scholar
  60. 60.
    van Griensven, L. J. (2000). Science and cultivation of edible fungi. Milton Park: Taylor & Francis.Google Scholar
  61. 61.
    Wang, H., & Ng, T. (2004). A new laccase from dried fruiting bodies of the monkey head mushroom Hericium erinaceum. Biochem Bioph Res Co, 322, 17–21.CrossRefGoogle Scholar
  62. 62.
    Wu, S., Yu, X., Hu, Z., Zhang, L., & Chen, J. (2009). Optimizing aerobic biodegradation of dichloromethane using response surface methodology. Journal of Environmental Sciences, 21, 1276–1283.CrossRefGoogle Scholar
  63. 63.
    Xiao, L.-P., Shi, Z.-J., Bai, Y.-Y., Wang, W., Zhang, X.-M., & Sun, R.-C. (2013). Biodegradation of lignocellulose by white-rot fungi: structural characterization of water-soluble hemicelluloses. Bioenergy Research, 6, 1154–1164.CrossRefGoogle Scholar
  64. 64.
    Zervakis, G., Philippoussis, A., Ioannidou, S., & Diamantopoulou, P. (2001). Mycelium growth kinetics and optimal temperature conditions for the cultivation of edible mushroom species on lignocellulosic substrates. Folia Microbiologica, 46, 231–234.CrossRefGoogle Scholar
  65. 65.
    Zhang, Z. F., Lv, G. Y., Pan, H. J., Pandey, A., He, W. Q., & Fan, L. F. (2012). Antioxidant and hepatoprotective potential of endo-polysaccharides from Hericium erinaceus grown on tofu whey. International Journal of Biological Macromolecules, 51, 1140–1146.CrossRefGoogle Scholar
  66. 66.
    Zjalic, S., Reverberi, M., Ricelli, A., Granito, V. M., Fanelli, C., & Fabbri, A. A. (2006). Trametes versicolor: a possible tool for aflatoxin control. International Journal of Food Microbiology, 107, 243–249.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Jangwoo Lee
    • 1
  • Seung Gu Shin
    • 1
  • Jinmo Ahn
    • 1
    • 2
  • Gyuseong Han
    • 1
  • Kwanghyun Hwang
    • 3
  • Woong Kim
    • 4
  • Seokhwan Hwang
    • 1
    Email author
  1. 1.School of Environmental Science and EngineeringPohang University of Science and Technology (POSTECH)PohangRepublic of Korea
  2. 2.Division of Advanced Nuclear EngineeringPOSTECHPohangRepublic of Korea
  3. 3.Environmental Process Engineering Team, Global Engineering Division, GS E&CSeoulRepublic of Korea
  4. 4.Department of Environmental EngineeringKyungpook National UniversityDaeguSouth Korea

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