Main Article Content
Abstract
Spent mushroom substrate (SMS) is widely used as fertilizer and to control plant diseases. The microorganisms surviving in SMS play a crucial role in plant growth promotion and biocontrol properties of SMS. In this study, an effort was made to isolate and characterize the bacterial species present in the SMS of Agaricus bisporus and to study their antagonistic potential, plant growth-promoting ability and indole-3-acetic acid (IAA) producing trait. Six different bacterial isolates exhibiting morphological variabilities were obtained from the SMS by serial dilution technique. On the basis of 16S rRNA gene sequences, these isolates were identified as Staphylococcus epidermidis (Sh1 and Sh3), S. aureus (Sh2), Bacillus albus (Sh4), Delftia lacustris (Sh6) and Comamonas aquatica (Sh7). These bacterial strains were assayed for their antagonism against Pythium aphanidermatum, a phytopathogenic oomycete. The results of in vitro dual culture assay revealed that all the 6 bacterial isolates showed low levels of suppression of P. aphanidermatum and recorded less than 5 mm inhibition zone. Among the bacterial isolates, S. epidermidis Sh3 recorded the maximum inhibition zone of 4.2 mm. Plant growth promotion test using roll paper towel method revealed that C. aquatica Sh7, B. albus Sh4, D. lacustris Sh6 and S. epidermidis Sh3 caused a significant increase in seedling vigour of cucumber compared to control. The seeds treated with the bacterial isolate C. aquatica Sh7 showed the maximum seedling vigor. Assessment of in vitro production of IAA by the bacterial isolates revealed that the bacterial isolates highly varied (ranging from 0.28 to 9.25 mg L-1) in their potential for production of IAA. The maximum amount of IAA was produced by C. aquatica Sh7 (9.25 mg L-1), while the minimum was produced by S. epidermidis Sh1 (0.28 mg L-1).
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Article Details
References
- Ahlawat OP, Vijay B. 2010. Potential of thermophilic bacteria as microbial inoculant for commercial scale white button mushroom (Agaricus bisporus) compost production. Journal of Scientific and Industrial Research. 69: 948-955.
- Ahlawat OP, Manikandan K, Sagar MP, Raj D, Gupta P, Vijay B. 2011. Effect of composted button mushroom spent substrate on yield, quality and disease incidence of Pea (Pisum sativum). Mushroom Research. 20: 87-94.
- Al-Hussini HS, Al-Rawahi AY, Al-Marhoon AA, Al-Abri SA, Al-Mahmooli IH, Al- Sadi AM, Velazhahan R. 2019. Biological control of damping-off of tomato caused by Pythium aphanidermatum by using native antagonistic rhizobacteria isolated from Omani soil. Journal of Plant Pathology. 101: 315-322.
- Al-Shibli H, Dobretsov S, Al-Nabhani A, Maharachchikumbura SSN, Rethinasamy V, Al-Sadi AM. 2019. Aspergillus terreus obtained from mangrove exhibits antagonistic activities against Pythium aphanidermatum-induced damping-off of cucumber. PeerJ 7:e7884.
- Albertsen M, Karst SM, Ziegler AS, Kirkegaard RH, Nielsen PH. 2015. Back to basics- The influence of DNA extraction and primer choice on phylogenetic analysis of activated sludge communities. PLOS ONE. 10: e0132783.
- Asghar H, Zahir Z, Arshad M, Khaliq A. 2002. Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biology and Fertility of Soils. 35: 231-237.
- Boulter JI, Trevors JT, Boland GJ. 2002. Microbial studies of compost: bacterial identification, and their potential for turf- grass pathogen suppression. World Journal of Microbiology and Biotechnology. 18: 661-671.
- Cao G, Song T, Shen Y, Jin Q, Feng W, Fan L, Cai W. 2019. Diversity of bacterial and fungal communities in wheat straw compost for Agaricus bisporus cultivation. HortScience. 54: 100-109.
- Chin CFS, Furuya Y, Zainudin MHM, Ramli N, Hassan MA, Tashiro Y, Sakai K. 2017. Novel multifunctional plant growth–promoting bacteria in co-compost of palm oil industry waste. Journal of Bioscience and Bioengineering. 124: 506-513.
- Choudhary DK. 2011. First preliminary report on isolation and characterization of novel Acinetobacter spp. in casing soil used for cultivation of button mushroom, Agaricus bisporus (Lange) Imbach. International Journal of Microbiology. 2011. Article ID 790285.
- Deepa CK, Dastager SG, Pandey A. 2010. Isolation and characterization of plant growth promoting bacteria from non-rhizospheric soil and their effect on cowpea (Vigna unguiculata (L.) Walp.) seedling growth. World Journal of Microbiology and Biotechnology. 26:1233-1240.
- Desbrosses G, Contesto C, Varoquaux F, Galland M, Touraine B. 2009. PGPR-Arabidopsis interactions is a useful system to study signaling pathways involved in plant developmental control. Plant Signaling & Behavior. 4: 319-321.
- Feeney MJ, Miller AM, Roupas P. 2014. Mushrooms-biologically distinct and nutritionally unique: exploring a “third food kingdom”. Nutrition Today. 49: 301-307.
- Gbolagade JS. 2006. Bacteria associated with compost used for cultivation of Nigerian edible mushrooms Pleurotus tuber-regium (Fr.) Singer, and Lentinus squarrosulus (Berk.). African Journal of Biotechnology. 5: 338-342.
- Gomes IP, Matos ADM, Nietsche S, Xavier AA, Costa MR, Gomes WS, Cristian M, Pereira T. 2017. Auxin production by endophytic bacteria isolated from banana trees. Brazilian Archives of Biology and Technology. 60: p.e17160484.
- Goonani Z, Sharifi K, Riahi H. 2011. The effects of spent mushroom compost and municipal solid waste compost on Phytophthora drechsleri in vivo and in vitro. Archives of Phytopathology and Plant Protection. 44: 1171-1181.
- Hanafi FHM, Rezania S, Taib SM, Din MFM, Yamauchi M, Sakamoto M, Hara H, Park J, Ebrahimi SS. 2018. Environmentally sustainable applications of agro-based spent mushroom substrate (SMS): an overview. Journal of Material Cycles and Waste Management. 20: 1383-1396.
- Inagaki R, Yamaguchi A. 2009. Spent substrate of shiitake (Lentinula edodes) inhibits symptoms of anthracnose in cucumber. Mushroom Science and Biotechnology. 17: 113-115.
- Kang DS, Min KJ, Kwak AM, Lee SY, Kang HW. 2017. Defense response and suppression of Phytophthora blight disease of pepper by water extract from spent mushroom substrate of Lentinula edodes. Plant Pathology Journal. 33: 264-275.
- Kertesz MA, Thai M. 2018. Compost bacteria and fungi that influence growth and development of Agaricus bisporus and other commercial mushrooms. Applied Microbiology and Biotechnology. 102: 1639-1650.
- Kwak AM, Kang DS, Lee SY, Kang HW. 2015. Effect of spent mushroom substrates on Phytophthora blight disease and growth promotion of pepper. Journal of Mushroom. 13: 16-20.
- Maniruzzaman M, Haque AU, Nasiruddin KM. 2008. Effect of growth hormone on the mycelial growth and spawn production in Oyster mushroom. Bangladesh Journal of Agricultural Research. 33: 51-58.
- Ntougias S, Zervakis GI, Kavroulakis N, Ehaliotis C, Papadopoulou KK. 2004. Bacterial diversity in spent mushroom compost assessed by amplified rDNA restriction analysis and sequencing of cultivated isolates. Systematic and Applied Microbiology. 27: 746-754.
- Parada RY, Murakami S, Shimomura N, Otani H. 2012. Suppression of fungal and bacterial diseases of cucumber plants by using the spent mushroom substrate of Lyophyllum decastes and Pleurotus eryngii. Journal of Phytopathology. 160: 390-396.
- Parada RY, Murakami S, Shimomura N, Egusa M, Otani H. 2011. Autoclaved spent substrate of hatakeshimeji mushroom (Lyophyllum decastes Sing) and its water extract protect cucumber from anthracnose. Crop Protection. 30: 443-450.
- Patten CL, Glick BR. 1996. Bacterial biosynthesis of indole-3-acetic acid. Canadian Journal of Microbiology. 42: 207-220.
- Persello‐Cartieaux F, Nussaume L, Robaglia C. 2003. Tales from the underground: molecular plant–rhizobacteria interactions. Plant, Cell & Environment. 26: 189-199.
- Rainey PB, Cole ALJ, Fermor TR, Wood DA. 1990. A model system for examining involvement of bacteria in basidiome initiation of Agaricus bisporus. Mycological Research. 94: 191-195.
- Ramachela K, Sihlangu SM. 2016. Effects of various hormonal treated plant substrates on development and yield of Pleurotus ostreatus. Cogent Food & Agriculture. 2: 1276510.
- Riahi H, Hashemi M, Sharifi K. 2012. The effect of spent mushroom compost on Lecanicillium fungicola in vivo and in vitro. Archives of Phytopathology and Plant Protection. 45: 2120-2131.
- Roy S, Barman S, Chakraborty U, Chakraborty B. 2015. Evaluation of spent mushroom substrate as biofertilizer for growth improvement of Capsicum annuum L. Journal of Applied Biology and Biotechnology. 3: 022-027.
- Schwachtje J, Karojet S, Kunz S, Brouwer S, van Dongen JT. 2012. Plant-growth promoting effect of newly isolated rhizobacteria varies between two Arabidopsis ecotypes. Plant signaling & behavior. 7: 623-627.
- Shifa H, Gopalakrishnan C, Velazhahan R. 2015. Efficacy of Bacillus subtilis G1 in suppression of stem rot caused by Sclerotium rolfsii and growth promotion of groundnut. International Journal of Agriculture Environment and Biotechnology. 8: 91-98.
- Silva CF, Azevedo RS, Braga C, Silva RD, Dias ES, Schwan RF. 2009. Microbial diversity in a bagasse-based compost prepared for the production of Agaricus brasiliensis. Brazilian Journal of Microbiology. 40: 590-600.
- Sreevidya M, Gopalakrishnan S. 2017. Direct and indirect plant growth-promoting abilities of Bacillus species on chickpea, isolated from compost and rhizosphere soils. Organic Agriculture. 7: 31-40.
- Straatsma G, Olijnsma TW, Gerrits JPG, Amsing JGM, Op den Camp HJM, Van Griensven LJLD. 1994. Inoculation of Scytalidium thermophilum in button mushroom compost and its effect on yield. Applied and Environmental Microbiology. 60: 3049-3054
- Suarez-Estrella F, Vargas-Garcıa C, Lopeza MJ, Capelb C, Morenoa J. 2007. Antagonistic activity of bacteria and fungi from horticultural compost against Fusarium oxysporum f. sp. melonis. Crop Protection. 26: 46-53.
- Szkop M, Bielawski W. 2013. A simple method for simultaneous RP-HPLC determination of indolic compounds related to bacterial biosynthesis of indole-3-acetic acid. Antonie Van Leeuwenhoek. 103: 683-691.
- Uzun I. 2004. Use of spent mushroom compost in sustainable fruit production. Journal of Fruit and Ornamental Plant Research. 12: 157-165.
- 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 Management. 24: 81-86.
- Yohalem D, Nordheim E, Andrews J. 1996. The effect of water extracts of spent mushroom compost on apple scab in the field. Phytopathology. 86: 914-922.
- Zhu D, Xie C, Huang Y, Sun J, Zhang, W. 2014. Description of Comamonas serinivorans sp. nov., isolated from wheat straw compost. International Journal of Systematic and Evolutionary Microbiology. 64: 4141-4146.
References
Ahlawat OP, Vijay B. 2010. Potential of thermophilic bacteria as microbial inoculant for commercial scale white button mushroom (Agaricus bisporus) compost production. Journal of Scientific and Industrial Research. 69: 948-955.
Ahlawat OP, Manikandan K, Sagar MP, Raj D, Gupta P, Vijay B. 2011. Effect of composted button mushroom spent substrate on yield, quality and disease incidence of Pea (Pisum sativum). Mushroom Research. 20: 87-94.
Al-Hussini HS, Al-Rawahi AY, Al-Marhoon AA, Al-Abri SA, Al-Mahmooli IH, Al- Sadi AM, Velazhahan R. 2019. Biological control of damping-off of tomato caused by Pythium aphanidermatum by using native antagonistic rhizobacteria isolated from Omani soil. Journal of Plant Pathology. 101: 315-322.
Al-Shibli H, Dobretsov S, Al-Nabhani A, Maharachchikumbura SSN, Rethinasamy V, Al-Sadi AM. 2019. Aspergillus terreus obtained from mangrove exhibits antagonistic activities against Pythium aphanidermatum-induced damping-off of cucumber. PeerJ 7:e7884.
Albertsen M, Karst SM, Ziegler AS, Kirkegaard RH, Nielsen PH. 2015. Back to basics- The influence of DNA extraction and primer choice on phylogenetic analysis of activated sludge communities. PLOS ONE. 10: e0132783.
Asghar H, Zahir Z, Arshad M, Khaliq A. 2002. Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biology and Fertility of Soils. 35: 231-237.
Boulter JI, Trevors JT, Boland GJ. 2002. Microbial studies of compost: bacterial identification, and their potential for turf- grass pathogen suppression. World Journal of Microbiology and Biotechnology. 18: 661-671.
Cao G, Song T, Shen Y, Jin Q, Feng W, Fan L, Cai W. 2019. Diversity of bacterial and fungal communities in wheat straw compost for Agaricus bisporus cultivation. HortScience. 54: 100-109.
Chin CFS, Furuya Y, Zainudin MHM, Ramli N, Hassan MA, Tashiro Y, Sakai K. 2017. Novel multifunctional plant growth–promoting bacteria in co-compost of palm oil industry waste. Journal of Bioscience and Bioengineering. 124: 506-513.
Choudhary DK. 2011. First preliminary report on isolation and characterization of novel Acinetobacter spp. in casing soil used for cultivation of button mushroom, Agaricus bisporus (Lange) Imbach. International Journal of Microbiology. 2011. Article ID 790285.
Deepa CK, Dastager SG, Pandey A. 2010. Isolation and characterization of plant growth promoting bacteria from non-rhizospheric soil and their effect on cowpea (Vigna unguiculata (L.) Walp.) seedling growth. World Journal of Microbiology and Biotechnology. 26:1233-1240.
Desbrosses G, Contesto C, Varoquaux F, Galland M, Touraine B. 2009. PGPR-Arabidopsis interactions is a useful system to study signaling pathways involved in plant developmental control. Plant Signaling & Behavior. 4: 319-321.
Feeney MJ, Miller AM, Roupas P. 2014. Mushrooms-biologically distinct and nutritionally unique: exploring a “third food kingdom”. Nutrition Today. 49: 301-307.
Gbolagade JS. 2006. Bacteria associated with compost used for cultivation of Nigerian edible mushrooms Pleurotus tuber-regium (Fr.) Singer, and Lentinus squarrosulus (Berk.). African Journal of Biotechnology. 5: 338-342.
Gomes IP, Matos ADM, Nietsche S, Xavier AA, Costa MR, Gomes WS, Cristian M, Pereira T. 2017. Auxin production by endophytic bacteria isolated from banana trees. Brazilian Archives of Biology and Technology. 60: p.e17160484.
Goonani Z, Sharifi K, Riahi H. 2011. The effects of spent mushroom compost and municipal solid waste compost on Phytophthora drechsleri in vivo and in vitro. Archives of Phytopathology and Plant Protection. 44: 1171-1181.
Hanafi FHM, Rezania S, Taib SM, Din MFM, Yamauchi M, Sakamoto M, Hara H, Park J, Ebrahimi SS. 2018. Environmentally sustainable applications of agro-based spent mushroom substrate (SMS): an overview. Journal of Material Cycles and Waste Management. 20: 1383-1396.
Inagaki R, Yamaguchi A. 2009. Spent substrate of shiitake (Lentinula edodes) inhibits symptoms of anthracnose in cucumber. Mushroom Science and Biotechnology. 17: 113-115.
Kang DS, Min KJ, Kwak AM, Lee SY, Kang HW. 2017. Defense response and suppression of Phytophthora blight disease of pepper by water extract from spent mushroom substrate of Lentinula edodes. Plant Pathology Journal. 33: 264-275.
Kertesz MA, Thai M. 2018. Compost bacteria and fungi that influence growth and development of Agaricus bisporus and other commercial mushrooms. Applied Microbiology and Biotechnology. 102: 1639-1650.
Kwak AM, Kang DS, Lee SY, Kang HW. 2015. Effect of spent mushroom substrates on Phytophthora blight disease and growth promotion of pepper. Journal of Mushroom. 13: 16-20.
Maniruzzaman M, Haque AU, Nasiruddin KM. 2008. Effect of growth hormone on the mycelial growth and spawn production in Oyster mushroom. Bangladesh Journal of Agricultural Research. 33: 51-58.
Ntougias S, Zervakis GI, Kavroulakis N, Ehaliotis C, Papadopoulou KK. 2004. Bacterial diversity in spent mushroom compost assessed by amplified rDNA restriction analysis and sequencing of cultivated isolates. Systematic and Applied Microbiology. 27: 746-754.
Parada RY, Murakami S, Shimomura N, Otani H. 2012. Suppression of fungal and bacterial diseases of cucumber plants by using the spent mushroom substrate of Lyophyllum decastes and Pleurotus eryngii. Journal of Phytopathology. 160: 390-396.
Parada RY, Murakami S, Shimomura N, Egusa M, Otani H. 2011. Autoclaved spent substrate of hatakeshimeji mushroom (Lyophyllum decastes Sing) and its water extract protect cucumber from anthracnose. Crop Protection. 30: 443-450.
Patten CL, Glick BR. 1996. Bacterial biosynthesis of indole-3-acetic acid. Canadian Journal of Microbiology. 42: 207-220.
Persello‐Cartieaux F, Nussaume L, Robaglia C. 2003. Tales from the underground: molecular plant–rhizobacteria interactions. Plant, Cell & Environment. 26: 189-199.
Rainey PB, Cole ALJ, Fermor TR, Wood DA. 1990. A model system for examining involvement of bacteria in basidiome initiation of Agaricus bisporus. Mycological Research. 94: 191-195.
Ramachela K, Sihlangu SM. 2016. Effects of various hormonal treated plant substrates on development and yield of Pleurotus ostreatus. Cogent Food & Agriculture. 2: 1276510.
Riahi H, Hashemi M, Sharifi K. 2012. The effect of spent mushroom compost on Lecanicillium fungicola in vivo and in vitro. Archives of Phytopathology and Plant Protection. 45: 2120-2131.
Roy S, Barman S, Chakraborty U, Chakraborty B. 2015. Evaluation of spent mushroom substrate as biofertilizer for growth improvement of Capsicum annuum L. Journal of Applied Biology and Biotechnology. 3: 022-027.
Schwachtje J, Karojet S, Kunz S, Brouwer S, van Dongen JT. 2012. Plant-growth promoting effect of newly isolated rhizobacteria varies between two Arabidopsis ecotypes. Plant signaling & behavior. 7: 623-627.
Shifa H, Gopalakrishnan C, Velazhahan R. 2015. Efficacy of Bacillus subtilis G1 in suppression of stem rot caused by Sclerotium rolfsii and growth promotion of groundnut. International Journal of Agriculture Environment and Biotechnology. 8: 91-98.
Silva CF, Azevedo RS, Braga C, Silva RD, Dias ES, Schwan RF. 2009. Microbial diversity in a bagasse-based compost prepared for the production of Agaricus brasiliensis. Brazilian Journal of Microbiology. 40: 590-600.
Sreevidya M, Gopalakrishnan S. 2017. Direct and indirect plant growth-promoting abilities of Bacillus species on chickpea, isolated from compost and rhizosphere soils. Organic Agriculture. 7: 31-40.
Straatsma G, Olijnsma TW, Gerrits JPG, Amsing JGM, Op den Camp HJM, Van Griensven LJLD. 1994. Inoculation of Scytalidium thermophilum in button mushroom compost and its effect on yield. Applied and Environmental Microbiology. 60: 3049-3054
Suarez-Estrella F, Vargas-Garcıa C, Lopeza MJ, Capelb C, Morenoa J. 2007. Antagonistic activity of bacteria and fungi from horticultural compost against Fusarium oxysporum f. sp. melonis. Crop Protection. 26: 46-53.
Szkop M, Bielawski W. 2013. A simple method for simultaneous RP-HPLC determination of indolic compounds related to bacterial biosynthesis of indole-3-acetic acid. Antonie Van Leeuwenhoek. 103: 683-691.
Uzun I. 2004. Use of spent mushroom compost in sustainable fruit production. Journal of Fruit and Ornamental Plant Research. 12: 157-165.
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 Management. 24: 81-86.
Yohalem D, Nordheim E, Andrews J. 1996. The effect of water extracts of spent mushroom compost on apple scab in the field. Phytopathology. 86: 914-922.
Zhu D, Xie C, Huang Y, Sun J, Zhang, W. 2014. Description of Comamonas serinivorans sp. nov., isolated from wheat straw compost. International Journal of Systematic and Evolutionary Microbiology. 64: 4141-4146.