Abstract
Background and aims
Spent mushroom substrates (SMSs) are widely used as organic fertilizer due to their high nutrients. However, the contribution of different types and amounts of SMSs to soil nutrients and microbial communities has been underreported. This study aims to provide data support for the selection and suitable application of SMSs, and to inform sustainable agricultural development.
Methods
The present study conducted a two-year field observation to investigate the effects of substituting 25% or 50% of chemical fertilizer (based on Nitrogen application) with Flammulina velutipes residue (FVR), Agaricus bisporus residue (ABR), and Auricularia auricula residue (AAR) on soil nutrients and microbial communities.
Results
Compared to chemical fertilizer treatment (CF), SMS treatments significantly increased soil organic carbon (OC) and carbon-nitrogen ratio (C/N) by 13.75–27.15% and 16.17–25.25%, respectively. The AAR treatment exhibited superior performance to other SMS treatments in improving soil nutrients. Notably, using AAR to replace 25% of chemical fertilizer (AAR1) was more effective than replacing 50% (AAR2) in enhancing nutrient availability. Compared to CF, the application of SMS significantly enhanced bacterial α-diversity without obviously affecting fungi. The relative abundance of Actinobacteria in AAR1 significantly decreased compared to CF. Furthermore, the application of SMS atered the proportions of bacterial and fungal functional groups. Finally, the application of SMS improved microbial diversity and altered microbial community composition by enhancing soil OC and C/N (especially AAR1).
Conclusions
This study crucially provides information on the application of SMS for nutrient amelioration and microbial community modulation, fostering a sustainable and resilient soil ecosystem.
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References
Ahmad R, Gao J, Li W et al (2023) Response of soil nutrients, enzyme activities, and fungal communities to biochar availability in the rhizosphere of mountainous apple trees. Plant Soil 489:277–293. https://doi.org/10.1007/s11104-023-06016-4
Akhtar K, Wang W, Ren G et al (2018) Changes in soil enzymes, soil properties, and maize crop productivity under wheat straw mulching in Guanzhong, China. Soil Tillage Res 182:94–102. https://doi.org/10.1016/j.still.2018.05.007
Barra PJ, Pontigo S, Delgado M et al (2019) Phosphobacteria inoculation enhances the benefit of P–fertilization on lolium perennein soils contrasting in P–availability. Soil Boil Biochem 136:107516. https://doi.org/10.1016/j.soilbio.2019.06.012
Bhattacharyya R, Rabbi SMF, Zhang Y et al (2021) Soil organic carbon is significantly associated with the pore geometry, microbial diversity and enzyme activity of the macro-aggregates under different land uses. Sci Total Environ 778:146286. https://doi.org/10.1016/j.scitotenv.2021.146286
Cao J, Wang H, Holden NM et al (2021) Soil properties and microbiome of annual and perennial cultivated grasslands on the Qinghai–Tibetan Plateau. Land Degrad Dev 32:5306–5321. https://doi.org/10.1002/ldr.4110
Chang EH, Chung RS, Tsai YH (2007) Effect of different application rates of organic fertilizer on soil enzyme activity and microbial population. Soil Sci Plant Nutr 53:132–140. https://doi.org/10.1111/j.1747-0765.2007.00122.x
Chen JS, Chiu CY (2003) Characterization of soil organic matter in different particle-size fractions in humid subalpine soils by CP/MAS 13 C-NMR. Geoderma 117:129–141. https://doi.org/10.1016/S0016-7061(03)00160-5
Chen S, Zhou Y, Chen Y et al (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):884–890. https://doi.org/10.1093/bioinformatics/bty560
Chen L, Zhou W, Luo L et al (2022) Short-term responses of soil nutrients, heavy metals and microbial community to partial substitution of chemical fertilizer with spent mushroom substrates (SMS). Sci Total Environ 844:157064. https://doi.org/10.1016/j.scitotenv.2022.157064
Chen SJ, Zhu Y, Shao TY et al (2019) Relationship between rhizosphere soil properties and disease severity in highbush blueberry (Vaccinium corymbosum). Appl Soil Ecol 137:187–194. https://doi.org/10.1016/j.apsoil.2019.02.015
Cheng J, Jing G, Wei L et al (2016) Long-term grazing exclusion effects on vegetation characteristics, soil properties and bacterial communities in the semi-arid grasslands of China. Ecol Eng 97:170–178. https://doi.org/10.1016/j.ecoleng.2016.09.003
Cuartero J, Pascual JA, Vivo JM et al (2022) A first-year melon/cowpea intercropping system improves soil nutrients and changes the soil microbial community. Agr Ecosyst Environ 328:107856. https://doi.org/10.1016/j.agee.2022.107856
Delgado-Baquerizo M, Maestre FT, Reich PB et al (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Díaz E, Jiménez JI, Nogales J (2013) Aerobic degradation of aromatic compounds. Curr Opin Biotech 24:431–442. https://doi.org/10.1016/j.copbio.2012.10.010
Dini-Andreote F, Stegen JC, Elsas JDV et al (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA 112:E1326–E1332. https://doi.org/10.1073/pnas.1414261112
Dominchin MF, Verdenelli RA, Berger MG et al (2021) Impact of N-fertilization and peanut shell biochar on soil microbial community structure and enzyme activities in a typic haplustoll under different management practices. Eur J Soil Biol 104:103298. https://doi.org/10.1016/j.ejsobi.2021.103298
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Fierer N, Lauber CL, Ramirez KS et al (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. https://doi.org/10.1038/ismej.2011.159
Gao W, Liang J, Pizzul L et al (2015) Evaluation of spent mushroom substrate as substitute of peat in Chinese biobeds. Int Biodeterior Biodegrad 98:107–112. https://doi.org/10.1016/j.ibiod.2014.12.008
Gao Y, Wang J, Ge Y et al (2024) Partial substitution of nitrogen fertilizers by organic products of rural waste co-composting impacts on farmland soil quality. Environ Technol Innov 33:103470. https://doi.org/10.1016/j.eti.2023.103470
Gobbi V, Nicoletto C, Zanin G et al (2018) Specific humus systems from mushrooms culture. Appl Soil Ecol 123:709–713. https://doi.org/10.1016/j.apsoil.2017.10.023
Goglio P, Ponsioen T, Carrasco J et al (2024) An environmental assessment of Agaricus Bisporus ((J.E.Lange) Imbach) mushroom production systems across Europe. Eur J Agron 155:127108. https://doi.org/10.1016/j.eja.2024.127108
Haack SK, Garchow H, Odelson DA et al (1994) Accuracy, reproducibility, and interpretation of fatty acid Methyl Ester profiles of Model Bacterial communities. Appl Environ Microb 60:2483–2493. https://doi.org/10.1128/aem.60.7.2483-2493.1994
Hafez M, Popov AI, Rashad M (2021) Integrated use of bio-organic fertilizers for enhancing soil fertility-plant nutrition, germination status and initial growth of corn (Zea mays L). Environ Technol Innov 21:101329. https://doi.org/10.1016/j.eti.2020.101329
Han J, Dong Y, Zhang M (2021) Chemical fertilizer reduction with organic fertilizer effectively improve soil fertility and microbial community from newly cultivated land in the loess plateau of China. Appl Soil Ecol 165:103966. https://doi.org/10.1016/j.apsoil.2021.103966
He L, Jing G, Zhao N et al (2023) Soil nutrients and the responses of microbial community structure to pine bark and vinegar residues in blueberry cultivation. Appl Soil Ecol 189:104907. https://doi.org/10.1016/j.apsoil.2023.104907
He J, Zhu N, Xu Y et al (2022) The microbial mechanisms of enhanced humification by inoculation with Phanerochaete chrysosporium and Trichoderma longibrachiatum during biogas residues composting. Bioresource Technol 351:126973. https://doi.org/10.1016/j.biortech.2022.126973
Jin X, Cai J, Yang S et al (2023) Partial substitution of chemical fertilizer with organic fertilizer and slow-release fertilizer benefits soil microbial diversity and pineapple fruit yield in the tropics. Appl Soil Ecol 189:104974. https://doi.org/10.1016/j.apsoil.2023.104974
Kim H-S, Lee S-H, Jo HY et al (2021) Diversity and composition of soil Acidobacteria and Proteobacteria communities as a bacterial indicator of past land-use change from forest to farmland. Sci Total Environ 797:148944. https://doi.org/10.1016/j.scitotenv.2021.148944
Kuramae EE, Costa OYA (2019) Acidobacteria. Encyclopedia of Microbiology, 4th edn. Academic Press, pp 1–8. https://doi.org/10.1016/B978-0-12-809633-8.20780-2
Küsel K, Drake HL (1998) Microbial turnover of low molecular weight organic acids during leaf litter decomposition. Soil Biol Biochem 31:107–118. https://doi.org/10.1016/S0038-0717(98)00111-4
Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371. https://doi.org/10.1016/j.soilbio.2010.04.003
Lauber CL, Strickland MS, Bradford MA et al (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. https://doi.org/10.1016/j.soilbio.2008.05.021
Lehmann J, Rilling MC, Thies J et al (2011) Biochar effects on soil biota - A review. Soil Biol Biochem 43:1812–1836. https://doi.org/10.1016/j.soilbio.2011.04.022
Leong YK, Ma T, Chang J et al (2022) Recent advances and future directions on the valorization of spent mushroom substrate (SMS): a review. Bioresour Technol 344:126157. https://doi.org/10.1016/j.biortech.2021.126157
Li S, Li Y, Hu C et al (2021) Stochastic processes drive bacterial and fungal community assembly in sustainable intensive agricultural soils of Shanghai, China. Sci Total Environ 778:146021. https://doi.org/10.1016/j.scitotenv.2021.146021
Liu X, Liu H, Zhang Y et al (2023) Straw return drives soil microbial community assemblage to change metabolic processes for soil quality amendment in a rice-wheat rotation system. Soil Biol Biochem 185:109131. https://doi.org/10.1016/j.soilbio.2023.109131
Liu Q, Pang Z, Sun H et al (2024) Unveiling the maize-benefit: synergistic impacts of organic-inorganic fertilizer cooperation on rhizosphere microorganisms and metabolites. Appl Soil Ecol 193:105171. https://doi.org/10.1016/j.apsoil.2023.105171
Lundquist EJ, Jackson LE, Scow KM et al (1999) Changes in microbial biomass and community composition, and soil carbon and nitrogen pools after incorporation of rye into three California agricultural soils. Soil Biol Biochem 31:221–236. https://doi.org/10.1016/S0038-0717(98)00093-5
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Maltas A, Kebli H, Oberholzer HR et al (2017) The effects of organic and mineral fertilizers on carbon sequestration, soil properties, and crop yields from a long-term field experiment under a Swiss conventional farming system. Land Degrad Dev 29(4):926–938. https://doi.org/10.1002/ldr.2913
Medina E, Paredes C, Bustamante MA et al (2012) Relationships between soil physico-chemical, chemical and biological properties in a soil amended with spent mushroom substrate. Geoderma 173–174:152–161. https://doi.org/10.1016/j.geoderma.2011.12.011
Moreira H, Pereira SI, Vega A et al (2020) Synergistic effects of arbuscular mycorrhizal fungi and plant growth-promoting bacteria benefit maize growth under increasing soil salinity. J Environ Manag 257:109982. https://doi.org/10.1016/j.jenvman.2019.109982
Najafi B, Faizollahzadeh Ardabili S, Shamshirband S, Chau K-W (2019) Spent mushroom compost (SMC) as a source for biogas production in Iran. Eng Appl Comp Fluid 13(1):967–982. https://doi.org/10.1080/19942060.2019.1658644
Nelson CE, Carlson CA (2012) Tracking differential incorporation of dissolved organic carbon types among diverse lineages of Sargasso Sea bacterioplankton. Environ Microbiol 14:1500–1516. https://doi.org/10.1111/j.1462-2920.2012.02738.x
Paula FS, Tatti E, Abram F et al (2017) Stabilisation of spent mushroom substrate for application as a plant growth-promoting organic amendment. J Environ Manag 196:476–486. https://doi.org/10.1016/j.jenvman.2017.03.038
Probst M, Gómez-Brandón M, Herbón C et al (2023) Fungal-bacterial associations in urban allotment garden soils. Appl Soil Ecol 188:104896. https://doi.org/10.1016/j.apsoil.2023.104896
Rai D, Silveira M, Strauss S et al (2023) Short-term prescribed fire-induced changes in soil microbial communities and nutrients in native rangelands of Florida. Appl Soil Ecol 189:104914. https://doi.org/10.1016/j.apsoil.2023.104914
Ren J, Liu X, Yang W et al (2021) Rhizosphere soil properties, microbial community, and enzyme activities: short-term responses to partial substitution of chemical fertilizer with organic manure. J Environ Manag 299:113650. https://doi.org/10.1016/j.jenvman.2021.113650
Royse DJ, Baars J, Tan Q (2017) Current overview of mushroom production in the world. Edible Med Mushrooms Technol Appl 5–13. https://doi.org/10.1002/9781119149446.ch2
Saxena G, Bharagava RN, Kaithwas G et al (2015) Microbial indicators, pathogens and methods for their monitoring in water environment. J Water Health 13:319–339. https://doi.org/10.2166/wh.2014.275
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: Open-Source, Platform-Independent, community-supported Software for describing and comparing Microbial communities. Appl Environ Microb 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Shakoor A, Shakoor S, Rehman A et al (2021) Effect of animal manure, crop type, climate zone, and soil attributes on greenhouse gas emissions from agricultural soils-a global meta-analysis. J Clean Prod 278:124019. https://doi.org/10.1016/j.jclepro.2020.124019
Soumare A, Boubekri K, Lyamlouli K et al (2021) Efficacy of phosphate solubilizing actinobacteria to improve rock phosphate agronomic effectiveness and plant growth promotion. Rhizosphere 17:100284. https://doi.org/10.1016/j.rhisph.2020.100284
Su J, Ji W, Sun X et al (2023) Effects of different management practices on soil microbial community structure and function in alpine grassland. J Environ Manag 327:116859. https://doi.org/10.1016/j.jenvman.2022.116859
Sun C, Wei Y, Kou J et al (2021) Improve spent mushroom substrate decomposition, bacterial community and mature compost quality by adding cellulase during composting. J Clean Prod 299:126928. https://doi.org/10.1016/j.jclepro.2021.126928
Tao Z, Liu X, Sun L et al (2022) Effects of two types nitrogen sources on humification processes and phosphorus dynamics during the aerobic composting of spent mushroom substrate. J Environ Manag 317:115453. https://doi.org/10.1016/j.jenvman.2022.115453
Udom BE, Nuga BO, Adesodun JK (2016) Water-stable aggregates and aggregate-associated organic carbon and nitrogen after three annual applications of poultry manure and spent mushroom wastes. Appl Soil Ecol 101:5–10. https://doi.org/10.1016/j.apsoil.2016.01.007
Vitousek PM, Naylor R, Crews T et al (2009) Nutrient imbalances in agricultural development. Science 324:1519–1520. https://doi.org/10.1126/science.1170261
Wang H, Xu M, Cai X et al (2020) Application of spent mushroom substrate suppresses fusarium wilt in cucumber and alters the composition of the microbial community of the cucumber rhizosphere. Eur J Soil Biol 101:103245. https://doi.org/10.1016/j.ejsobi.2020.103245
Wardle DA, Bardgett RD, Klironomos JN et al (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. https://doi.org/10.1126/science.1094875
Yan T, Xue J, Zhou Z et al (2021) Biochar-based fertilizer amendments improve the soil microbial community structure in a karst mountainous area. Sci Total Environ 794:148757. https://doi.org/10.1016/j.scitotenv.2021.148757
Yang W, Li C, Wang S et al (2021) Influence of biochar and biochar-based fertilizer on yield, quality of tea and microbial community in an acid tea orchard soil. Appl Soil Ecol 166:104005. https://doi.org/10.1016/j.apsoil.2021.104005
Zhou R, Wang Y, Tian M et al (2021) Mixing of biochar, vinegar and mushroom residues regulates soil microbial community and increases cucumber yield under continuous cropping regime. Appl Soil Ecol 161:103883. https://doi.org/10.1016/j.apsoil.2021.103883
Zhu J, Peng H, Ji X et al (2019) Effects of reduced inorganic fertilization and rice straw recovery on soil enzyme activities and bacterial community in double-rice paddy soils. Eur J Agron 94:103116. https://doi.org/10.1016/j.ejsobi.2019.103116
Acknowledgements
This study was financially supported by the National Key Research and Development Program of China (Grant Nos. 2022YFC3204004 and 2023YFF1305203), the Strategic Research and Consulting Project of Chinese Academy of Engineering (Grant No. 2023-DFZD-31).
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Ludan Chen and Wei Zhou contributed to the study conception and design. Material preparation, data collection and analysis were performed by Ludan Chen. The first draft of the manuscript was written by Ludan Chen and Wei Zhou. The manuscript was revised by Chen Ludan, Bao Yuhai, He Xiubin and Deng Liangji. All authors read and approved the final manuscript.
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Chen, L., Bao, Y., Zhou, W. et al. Responses of soil nutrients and microbial communities to the application of spent mushroom substrates. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06679-7
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DOI: https://doi.org/10.1007/s11104-024-06679-7