A multifaceted analysis of spent mushroom substrate of selected oyster mushrooms for enzymatic activity, proximate composition, and antimicrobial activity
Main Article Content
Keywords
biofertilizer, lignocellulosic enzymes, spent mushroom substrate, P. djamor, P. ostreatus
Abstract
The global market for mushrooms is growing due to its nutritional enrichment, potential usage as a bioremediation, enzyme production, and functional food development. However, the leftover post-harvest mushroom substrate (SMS) generates certain environmental concerns. This study aimed to investigate the potential of SMS obtained from two oyster mushroom species—Pleurotus ostreatus and Pleurotus djamor. These were examined regarding sustainability by analyzing their lignocellulosic enzyme production, cellulose yield, antimicrobial properties, and proximate composition. The findings for both P. ostreatus and P. djamor showed higher activity of amylase, that is, 0.3 U (μmol/min) and 0.7 U (μmol/min), respectively, compared to activity of cellulase, which showed 0.3 U (μmol/min) and 0.5 U (μmol/min), respectively. SMS showed the highest activity of lignocellulosic enzymes, compared to non-SMCs and controls at p ≤ 0.00 and ≤0.01), proving fungual mycelia as the precursor of enzymes activity, as no mushroom is cultivated due to least enzymatic activity. The results for proximate analysis of SMCs showed a significant difference from non-SMCs. The findings for P. djmor revealed protein (1.23%), fats (1.3%), and ash (8.11), which were significantly higher than in P. ostreatus. A positive co-relation of 52% was established between SMCs with amylase, while a correlation of 20% was observed with cellulase, depicting an impact of mycelia in the breakdown of protein for amylase production. The SMC samples were also subjected to antibacterial analysis against Staphylococcus aureus, E. coli, and Xanthomonas. A higher minimum inhibition concentration (MIC) was recorded for P. djamor, that is, 8.80 mm, 11.66 mm, and 9.04 mm, compared to P. ostreatus, which showed its highest MIC as 9.18 mm, 9.30 mm, and 9.28 mm for S. aureus, E. coli, and Xanthomonas, respectively. It was evident from the study that SMC has a potential of being utilized for bioremediation, as it is therapeutically active against pathogens. Additionally, Pleurotus spp. is of great interest because of its ability to produce high nutritive value, cellulose yield, and a vast amount of lignocellulosic enzymes. The current experiment recommends the use of distilled water for mushroom farming, as enzymatic activities can significantly be affected by pH and buffers. Furthermore, the spent compost, being rich nutritionally, can be used for soil enrichment or as a biofertilizer.
References
Ahlawat O.P. and Sagar M.P. 2007. Management of Spent Mushroom Substrate. National Research Centre for Mushroom, Indian Council of Agricultural Research, New Delhi, India.
Ahmad B, Muhammad Yousafzai A, Maria H, Khan AA, Aziz T, Alharbi M, et al. 2023. Curative Effects of Dianthus orientalis against Paracetamol Triggered Oxidative Stress, Hepatic and Renal Injuries in Rabbit as an Experimental Model. Separations. 10(3):182. 10.3390/separations10030182
AOAC (2004) Official Methods of Analysis (15th edition). Association of official analytical chemists, Washington, D. C., U.S.A
Arshadi N., Nouri H. and Moghimi H. 2023. Increasing the production of the bioactive compounds in medicinal mushrooms: an omics perspective. Microb Cell Factories. 22(1):1–34. 10.1186/s12934-022-02013-x
Aziz T, Ihsan F, Ali Khan A, Ur Rahman S, Zamani GY, Alharbi M, et al. 2023. Assessing the pharmacological and biochemical effects of Salvia hispanica (Chia seed) against oxidized Helianthus annuus (sunflower) oil in selected animals. Acta Biochim Pol. 27;70(1):211–218. 10.18388/abp.2020_6621
Caldas L.A., Zied D.C. and Sartorelli P. 2022. Dereplication of extracts from nutraceutical mushrooms pleurotus using molecular network approach. Food Chem. 370:131019. 10.1016/j.foodchem.2021.131019
Chowdhary P., More N., Yadav A. and Bharagava R.N. 2019. Ligninolytic enzymes: an introduction and applications in the food industry. In: Enzymes in Food Biotechnology. Academic Press pp. 181–195. 10.1016/B978-0-12-813280-7.00012-8
Dedousi M., Melanouri E.M. and Diamantopoulou P. 2023. Carposome productivity of Pleurotus ostreatus and Pleurotus eryngii growing on agro-industrial residues enriched with nitrogen, calcium salts and oils. Carbon Res Conver. 6(2):150–165. 10.1016/j.crcon.2023.02.001
Diamantopoulou P. and Philippoussis A. 2015. Cultivated mushrooms: preservation and processing. In: Handbook of Vegetable Preservation and processing, pp. 495–525.
Durán-Aranguren D.D., Meléndez-Melo J.P., Covo-Ospina M.C., Díaz-Rendón J., Reyes-Gutiérrez D.N., Reina L.C., Durán-Sequeda D. and Sierra R. 2021. Biological pretreatment of fruit residues using the genus Pleurotus: a review. Bioresour. Technol. Rep. 16:100849. 10.1016/j.biteb.2021.100849
Ejaz A, Jahangeer M, Mahmood Akhtar Z, Aziz T, Alharbi M, Alshammari A, et al. 2023. Characterization and gastroprotective effects of Rosa brunonii Lindl. fruit on gastric mucosal injury in experimental rats-A preliminary study. Acta Biochim Pol. 18;70(3):633–641. 10.18388/abp.2020_6772
Economou C.N., Diamantopoulou P.A. and Philippoussis A.N. 2017. Valorization of spent oyster mushroom substrate and laccase recovery through successive solid state cultivation of Pleurotus, Ganoderma, and Lentinula strains. Appl Microbiol Biotechnol. 101(12):5213–5222. 10.1093/femsle/fnaa060
Economou C.N., Philippoussis A.N. and Diamantopoulou P.A. 2020. Spent mushroom substrate for a second cultivation cycle of Pleurotus mushrooms and dephenolization of agro-industrial wastewaters. FEMS Microbiol Lett. 367(8):fnaa060.
Geetha D. Sivaprakasam K. 1998. Enzyme and sporophore production potential of oyster mushroom (Pleurotus spp.). Mushroom Research. 7(1).
Getachew A, Keneni A, Chawaka M. 2019. Production of oyster mushroom (Pleurotus ostreatus) on substrate composed from wheat straw, waste paper and cotton seed waste. International Journal of Micro and Biotechnol. 4(2):38–44. 10.11648/j.ijmb.20190402.12
Ghorai S., Banik S.P., Verma D., Chowdhury S., Mukherjee S. and Khowala S. 2009. Fungal biotechnology in food and feed processing. Food Res Int. 42(5–6):577–587. 10.1016/j.foodres.2009.02.019
Guo J., Zhang M. and Fang Z. 2022. Valorization of mushroom by-products: a review. J Sci Food Agric. 102(13):5593–5605. 10.1002/jsfa.11946
Gul R., Rahmatullah Q., Ali H., Bashir A., Ayaz A.K., Aziz T., et al. 2023. Phytochemical, Anitmicrobial, Radical Scavening and In-vitro biological activities of Teucurium stocksianum leaves. J. Chil. Chem. Soc. 68(1):5748–5754. Available at: https://www.jcchems.com/index.php/JCCHEMS/article/view/2295
Karimi K., Arzanlou M., Ahari A.B. and Ghazi M.M. 2015. Phenotypic and molecular characterization of the causal agent of chafer beetle mortality in the wheat fields of the Kurdistan province. Iran. J Plant Protect Res. 2015. 10.1515/jppr-2015-0031
Kumar M., Kumar P., Das P., Solanki R. and Kapur M.K. 2020. Potential applications of extracellular enzymes from Streptomyces spp. in various industries. Archives of Microbiol. 202:1597–1615. 10.1007/s00203-020-01898-9
Lavelli V., Proserpio C., Gallotti F., Laureati M. and Pagliarini E. 2018. Circular reuse of bio-resources: the role of Pleurotus spp. in the development of functional foods. Food Funct. 9(3):1353–1372. 10.1039/C7FO01747B
Leong Y.K., Ma T.W., Chang J.S. and Yang F.C. 2022. Recent advances and future directions on the valorization of spent mushroom substrate (SMS): a review. Bioresource Technol. 344:126157. 10.1016/j.biortech.2022.128012
Lin Y., Ge X. and Li Y. 2014. Solid-state anaerobic co-digestion of spent mushroom substrate with yard trimmings and wheat straw for biogas production. Bioresour Technol. 169:468–474. 10.1016/j.biortech.2014.07.020
Lohmousavi S.M., Abad H.H.S., Noormohammadi G. and Delkhosh B. 2020. Synthesis and characterization of a novel controlled release nitrogen-phosphorus fertilizer hybrid nanocomposite based on banana peel cellulose and layered double hydroxides nanosheets. Arabian J of Chem. 13(9):6977–6985. 10.1016/j.arabjc.2020.06.042
Lu L., Zhai X., Li X., Wang S., Zhang L., Wang L., et al. 2022. Met1-specific motifs conserved in OTUB subfamily of green plants enable rice OTUB1 to hydrolyse Met1 ubiquitin chains. Nature Communications. 13(1):4672. 10.1038/s41467-022-32364-3
Melanouri E.-M., Dedousi M. and Diamantopoulou P. 2022. Cultivating Pleurotus ostreatus and Pleurotus eryngii mushroom strains on agro-industrial residues in solid-state fermentation. Part I: screening for growth, endoglucanase, laccase and biomass production in the colonization phase. Carbon Resour Convers. 5:61–70. 10.1016/j.crcon.2021.12.004
Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry. 31:426–428. 10.1021/ac60147a030
Mwangi R.W., Macharia J.M., Wagara I.N. and Bence R.L. 2022. The antioxidant potential of different edible and medicinal mushrooms. Biomed. Pharmacother. 147:112621. 10.1016/j.biopha.2022.112621
Nureen Z., Tahira F., Muhammad H., Basit Z., Abid S., Tariq A., et al. 2023. In-Vivo and In-Silico analysis of Anti-Inflammatory, Analgesic, and Anti pyretic activities of Citrus paradisi Leaf Extract. J. Chil. Chem. Soc. 68(2):5813–5821.
Prokisch J., Törős G. and El-Ramady H. 2021. Edible mushroom of Pleurotus spp.: a case study of oyster mushroom (Pleurotus ostreatus L.). EBSS 5:1–2.
Rajavat A.S., Mageshwaran V., Bharadwaj A., Tripathi S. and Pandiyan K. 2022. Spent mushroom waste: an emerging bio-fertilizer for improving soil health and plant productivity. In: New and Future Developments in Microbial Biotechnology and Bioengineering (pp. 345–354). Elsevier. 10.1016/B978-0-323-85579-2.00010-1
Rauf B., Alyasi S., Zahra N., Ahmad S., Sarwar A., Aziz T., et al. 2023. Evaluating the influence of Aloe barbadensis extracts on edema induced changes in C-reactive protein and interleukin-6 in albino rats through in vivo and in silico approaches. Acta Biochim Pol. 17;70(2):425–433. 10.18388/abp.2020_6705
Ranjithkumar M., Uthandi S., Senthil Kumar P., Muniraj I., Thanabal V. and Rajarathinam R. 2022. Highly crystalline cotton spinning wastes utilization: pretreatment, optimized hydrolysis and fermentation using Pleurotus florida for bioethanol production. Fuel. 308:122052. 10.1016/j.fuel.2021.122052
Salmones D., Mata G. and Waliszewski K.N. 2005. Comparative culturing of Pleurotus spp. on coffee pulp and wheat straw: biomass production and substrate biodegradation. Bioresour. Technol. 96(5):537–544. 10.1016/j.biortech.2004.06.019
Sana, U.R., Rahman S., Zahid M., Khan A.A., Aziz T., Iqbal Z., et al. 2022. Hepatoprotective effects of walnut oil and Caralluma tuberculata against paracetamol in experimentally induced liver toxicity in mice. Acta Biochim Pol. 24;69(4):871–878. 10.18388/abp.2020_6387
Singh N. and Sohrab S. 2024. Algae and fungi-based micronutrients enrichment in food. In: Phytoremediation and Biofortification: Strategies for Sustainable Environmental and Health Management, p. 335. 10.1201/9781003402084-15
Sun X.F., Sun R.C., Tomkinson J. and Baird M.S. 2003. Preparation of sugarcane bagasse hemicellulosic succinates using NBS as a catalyst. Carbohydrate Polymers. 53(4):483–495. 10.1016/S0144-8617(03)00150-4
Syed W.A.S., Muhammad S.A., Mujaddad U.R., Azam H., Abid S., Aziz T., et al. 2023. In-Vitro Evaluation of Phytochemicals, Heavy Metals and Antimicrobial Activities of Leaf, Stem and Roots Extracts of Caltha palustris var. alba. J. Chil. Chem. Soc. 68(1):5807–5812. 10.4067/S0717-97072023000105807
Tassou C., Koutsoumanis K. and Nychas G.J.E. 2000. Inhibition of Salmonella enteritidis and Staphylococcus aureus in nutrient broth by mint essential oil. Food Research International. 33:273–280. 10.1016/S0963-9969(00)00047-8
Thomas G.V., Prabhu S.R., Reeny M.Z. and Bopaiah B.M. 1998. Evaluation of lignocellulosic biomass from coconut palm as substrate for cultivation of Pleurotus sajor-caju (Fr.) Singer. World J of Micro and Biotechnol. 14:879–882. 10.1023/A:1008881124903
Torres-Martínez B.D.M., Vargas-Sánchez R.D., Torrescano-Urrutia G.R., Esqueda M., Rodríguez-Carpena J.G., Fernández-López J., et al. 2022. Pleurotus genus as a potential ingredient for meat products. Foods. 11(6):779. 10.3390/foods11060779
Wang S., Li W., Liu L., Qi H. and You H. 2022. Biodegradation of decabromodiphenyl ethane (DBDPE) by white-rot fungus Pleurotus ostreatus: characteristics, mechanisms, and toxicological response. J. Hazard Mater. 424:127716. 10.1016/j.jhazmat.2021.127716
Zisopoulos F.K., Ramírez H.A.B., van der Goot A.J. and Boom R.M. 2016. A resource efficiency assessment of the industrial mushroom production chain: the influence of data variability. J Clean Prod. 126:394–408. 10.1016/j.jclepro.2016.03.066
Zhang T., Yu S., Pan Y., Li H., Liu X. and Cao J. 2023. Properties of texturized protein and performance of different protein sources in the extrusion process: A review. Food Res. Int. 174:113588. 10.1016/j.foodres.2023.113588
Zhang, S., Dongye, Z., Wang, L., Li, Z., Kang, M., Qian, Y., et al. 2023. Influence of environmental pH on the interaction properties of WP-EGCG non-covalent nanocomplexes. J Sci of Food and Agri. 103(11):5364–5375. 10.1002/jsfa.12611
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