Abstract
The aim of the present work was to evaluate the nematicidal potential of Flammulina velutipes and its spent mushroom compost. Additionally, the nematicidal activity of enzymes and metabolites was analyzed. Isolated F. velutipes and its SMC had significant nematicidal effect on Panagrellus sp. larvae. The percentages of reduction in relation to the control group were: 69, 57.5 and 70% for SMC and 56, 24.5 and 26.6% for the isolated fungus, for 24, 48 and 72 h, respectively. The active SMC crude extract showed nematicidal action with reduction percentages of 43 and 57% for 24 and 48 h of incubation, respectively. The boiled crude extract also showed nematicidal action, however, the reduction percentages were lower than those of the active extract. This demonstrated that the nematicidal action was due to enzyme activities and other metabolites. The results demonstrated that SMC, the isolated fungus, the crude extract and the boiled crude extract showed a significant percentage of reduction on Panagrellus sp. larvae. SMC evidenced a higher nematicidal activity than the isolated fungus. In addition, nematophagous activity of F. velutipes was observed for the first time.
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References
Abd-Elgawad MMM, Askary TH (2018) Fungal and bacterial nematicides in integrated nematode management strategies. Egypt J Biol Pest Control 28:74. https://doi.org/10.1186/s41938-018-0080-x
Akhtar M, Malik A (2000) Roles of organic soil amendments and soil organisms in biological control of plant parasitic nematodes: a review. Bioresour Technol 74:35–47. https://doi.org/10.1016/S0960-8524(99)00154-6
Aslam SS (2013) Organic management of root knot nematodes in tomato with spent mushroom compost. Sarhad J Agric 29:63–69
Ayres M, Ayres JRM, Ayres DL, Santos AS (2003) Aplicações estatísticas nas áreas de ciências biológicas. Belém: Sociedade civil mamirauá: Brasília CNPq, p 290
Bao HN, Ochiai Y, Ohshima T (2010) Antioxidative activities of hydrophilic extracts prepared from the fruiting body and spent culture medium of Flammulinavelutipes. Bioresour Technol 101:6248–6255. https://doi.org/10.1016/j.biortech.2010.03.026
Cairol J, Djian C, Pijarowski L (1989) Study of the nematocidal properties of the culture filtrate of the nematophagous fungus Paecilomyces lilacinus. Nematology 12:331–336
Degenkolb T, Vilcinskas A (2016) Metabolites from nematophagous fungi and nematicidal natural products from fungi as alternatives for biological control. Part II: metabolites from nematophagous basidiomycetes and non = nematophagous fungi. Appl Microbiol Biotechnol 100:3813–3824. https://doi.org/10.1007/s00253-015-7234-5
Dong Y, Cheng S, Qi G, Yang Z, Yin S, Chen G (2017) Antimicrobial and antioxidant activities of Flammulina velutipes polisacchrides and polysaccharide-iron(III) complex. Carbohydr Polym 161:26–32. https://doi.org/10.1016/j.carbpol.2016.12.069
Drechsler C (1941) Some hyphomycetes parasitic on free-living terricolous nematodes. Phytopathology 31:773–801
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
Genier HLA, Soares FEF, Queiroz JH, Gouveia AS, Araújo JV, Braga FR, Pinheiro IR, Kasuya MCM (2015) Activity of the fungus Pleurotus ostreatus and of its proteases on Panagrellus sp. larvae. Afr J Biotechnol 14:1496–1503. https://doi.org/10.5897/AJB2015.14447
Gomes APS, Ramos ML, Vasconcellos RS, Jensen JR, Vieira-Bressan MCR, Araujo JV (2000) In vitro activity of brazilian strains of the predatory fungi Artrhobotrys spp. on free-living nematodes and infective larvae of Haemonchus placei. Mem Inst Oswaldo Cruz 95:873–876. https://doi.org/10.1590/S0074-02762000000600023
Grimm D, Wösten HA (2018) Mushroom cultivation in the circular economy. Appl Microbiol Biotechnol 102:7795–7803. https://doi.org/10.1007/s00253-018-9226-8
Grujié M, Dojnov B, Potočnikc I, Duduk B, Vujčić Z (2015) Spent mushroom compost as substrate for the production of industrially important hydrolytic enzymes by fungi Trichoderma spp. and Aspergillus niger in solid state fermentation. Int Biodeterior Biodegrad 104:290–298. https://doi.org/10.1016/j.ibiod.2015.04.029
Hassan MA, Pham TH, Shi H, Zeng J (2012) Nematodes threats to global food security. Acta Agric Scand B 63:420–425. https://doi.org/10.1080/09064710.2013.794858
Ishihara A, Goto N, Kikkawa M, Ube N, Ushijima S, Ueno M, Ueno K, Osaki-Oka K (2018) Identification of antifungal compounds in the spent mushroom substrate of Lentinula edodes. J Pest Sci 43:108–113. https://doi.org/10.1584/jpestics.D17-094
Jing P, Zhao SJ, Lu MM, Cai Z, Pang J, Song LH (2014) Multiple-fingerprint analysis for investigating quality control of Flammulina velutipes fruiting body polysaccharides. J Agric Food Chem 62:12128–12133. https://doi.org/10.1021/jf504349r
Kleyn JG, Wetzler TF (1981) The microbiology of spent mushroom compost and its dust. Can J Microbiol 27:748–753. https://doi.org/10.1139/m81-116
Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52:1539–1546. https://doi.org/10.1016/S0045-6535(03)00493-4
Leifa F, Pandey A, Soccol CR (2001) Production of Flammulina velutipes on coffee husk and coffee spent-ground. Braz Arch Biol Technol 44:205–212. https://doi.org/10.1590/S1516-89132001000200015
Leung MYK, Fung KP, Choy YM (1997) The isolation and characterization of an immunomodulatory and anti-tumor polysaccharide preparation from Flammulina velutipes. Immunopharmacol 35:255–263. https://doi.org/10.1016/S0162-3109(96)00157-9
Lopez-Llorca LV, Maciá-Vicente JG, Jansson HB (2008) Mode of action and interactions of nematophagous fungi. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Integrated management of plant pests and diseases, vol 2. Springer, Dordrecht, pp 52–76. https://doi.org/10.1007/978-1-4020-6063-2_3
Luo X, Yuan X, Wang S, Sun F, Hou Z, Hu Q, Zhai L, Cui Z, Zou Y (2018) Methane production and characteristics of the microbial community in the co-digestion of spent mushroom substrate with dairy manure. Bioresour Technol 250:611–620. https://doi.org/10.1016/j.biortech.2017.11.088
Nakamura M, Iketani A, Shioi Y (2011) A survey of proteases in edible mushrooms with synthetic peptides as substrates. Mycoscience 52:234–241. https://doi.org/10.1007/S10267-010-0089-9
Nakajima VM, Soares FEF, Queiroz JH (2018) Screening and decolorizing potential of enzymes from spent mushroom composts of six different mushrooms. Biocatal Agr Biotechnol 13:58–61. https://doi.org/10.1016/j.bcab.2017.11.011
Nordbring-Hertz B, Jansson H, Tunlind A (2011) Nematophagous fungi. Encycl Life Sci. https://doi.org/10.1002/9780470015902.a0000374.pub3
Rathore H, Prasad S, Sharma S (2017) Mushroom nutraceuticals for improved nutrition and better human health: a review. Pharmanutrition 5:35–46. https://doi.org/10.1016/j.phanu.2017.02.001
Redhead SA, Petersen RH (1999) New species, varieties and combinations in the genus Flammulina. Mycotaxon 71:285–294
Ribas LCC, Mendonça MM, Camelini CM, Soares CHL (2009) Use of spent mushroom substrates from Agaricus subrufescens (syn. A. blazei, A. brasiliensis) and Lentinula edodes productions in the enrichment of a soil-based potting media for lettuce (Lactuca sativa) cultivation: growth promotion and soil bioremediation. Bioresour Technol 100:4750–4757. https://doi.org/10.1016/j.biortech.2008.10.059
Royse DJ, Baars J, Tan Q (2017) Current overview of mushroom production in the world. In: Zied DC, Pardo-Giminez A (eds) Edibleand medicinal mushrooms: technology and applications. Wiley, Hoboken, pp 5–13. https://doi.org/10.1002/9781119149446.ch2
Siddiqui ZA, Mahmood I (1996) Biological control of plant parasitic nematodes by fungi: a review. Bioresour Technol 58:229–239. https://doi.org/10.1016/S0960-8524(96)00122-8
Soares FEF, Braga FR, Araújo JV, Geniêr HLA, Gouveia AS, Queiroz JH (2013) Nematicidal activity of three novel extracellular proteases of the nematophagous fungus Monacrosporium sinense. Parasitol Res 112:1557–1565. https://doi.org/10.1007/s00436-013-3304-8
Soares FEF, Sufiate BL, Queiroz JH (2018) Nematophagous fungi: far beyond the endoparasite, predator and ovicidal groups. ANRES 52:1–8. https://doi.org/10.1016/j.anres.2018.05.010
Soares FEF, Nakajima VM, Sufiate BL, Satiro LAS, Gomes EH, Fróes FV, Sena FP, Braga FB, Queiroz JH (2019) Proteolytic and nematicidal potential of the compost colonized by Hypsizygus marmoreus. Exp Parasitol 197:16–19. https://doi.org/10.1016/j.exppara.2018.12.006
Sufiate BL, Soares FEF, Moreira SS, Gouveia AS, Monteiro TSA, Freitas LG, Queiroz JH (2017) Nematicidal action of Pleurotus eryngii metabolites. Biocatal Agric Biotechnol 12:216–219. https://doi.org/10.1016/j.bcab.2017.10.009
Thorn RG, Barron GL (1984) Carnivorous mushrooms. Science 224:76–78. https://doi.org/10.1126/science.224.4644.76
Watabe M, Rao JR, Xu J, Millar BC, Ward RF, Moore JE (2004) Identification of novel eubacteria from spent mushroom compost (SMC) waste by DNA sequence typing: ecological considerations of disposal on agricultural land. Waste Manag 24:81–86. https://doi.org/10.1016/j.wasman.2003.08.001
Yildiz S, Yildiz ÜC, Gezer ED, Temiz A (2002) Some lignocellulosic wastes used as raw material in cultivation of the Pleurotus ostreatus culture mushroom. Process Biochem 38:301–306. https://doi.org/10.1016/S0032-9592(02)00040-7
Zhang L, Sun X (2014) Changes in physical, chemical, and microbiological properties during the two stage co-composition of green waste with spent mushroom compost and biochar. Bioresour Technol 171:274–284. https://doi.org/10.1016/j.biortech.2014.08.079
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The authors thank the National Council for Scientific and Technological Development (CNPq), the Coordination for the Improvement of Higher Education (CAPES) and Foundation for Supporting Research and Innovation in Espirito Santo (FAPES) for financial support.
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All authors prepared the manuscript. FEFS and FRB analyzed the data. All the experiments were designed by FEFS. All the experiments were executed by JMF and DNC.
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Ferreira, J.M., Carreira, D.N., Braga, F.R. et al. First report of the nematicidal activity of Flammulina velutipes, its spent mushroom compost and metabolites. 3 Biotech 9, 410 (2019). https://doi.org/10.1007/s13205-019-1951-x
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DOI: https://doi.org/10.1007/s13205-019-1951-x