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Spent mushroom substrate as a substitute for chemical fertilizer changes N-cycling genes and reduces N2O emission in different textured soils

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Abstract

Spent mushroom substrate (SMS) is a by-product of mushroom production, which can be used as an organic fertilizer. However, studies on the effect of SMS as a substitute for chemical fertilizer on soil N2O emissions and relative mechanisms are scarce. A laboratory incubation experiment was conducted to examine the effects of SMSs derived from Pleurotus eryngii (SMS-PE) and Agaricus bisporus (SMS-AB) production on N2O emissions from a sandy loam and a clay loam soil. Six treatments for each soil were established: no fertilization (CK); chemical N fertilizer (U); two types of SMSs alone (SMS-PE and SMS-AB); and their half substitution with chemical N fertilizer (SMS-PEU and SMS-ABU). The recalcitrance and aliphaticity indices of SMS-PE determined by 13C nuclear magnetic resonance spectra were lower than those of SMS-AB. N2O emissions from the SMS-PEU and SMS-ABU decreased by 21.5–58.5% compared to the urea alone treatment. The emission of N2O was controlled by soil NH4+-N and AOB, indicating that nitrification is primarily responsible for N2O production. The increased NH4+-N concentration in the SMS-PEU treatment increased N2O emissions by 32.4% compared to the SMS-ABU treatment of the sandy loam soil. The N2O emissions from the clay loam soil treated with SMS-PEU depended on NO3-N concentration and absolute abundance of nirS, nirK, and the nir/nos ratio, suggesting the presence of the simultaneous nitrification and denitrification. Thus, the application of SMS-PE with a higher proportion of available organic C increased denitrification gene abundance and likely enhanced denitrification-associated N2O emissions (by 72.6%) in the clay loam soil compared to SMS-ABU. Overall, our results reveal that substituting chemical N with SMSs, particularly SMS-AB with lower NH4+-N and available C concentrations, is a promising strategy to mitigate N2O emissions while reducing chemical N consumption.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Atallah E, Zeaiter J, Ahmad MN, Leahy JJ, Kwapinski W (2021) Hydrothermal carbonization of spent mushroom compost waste compared against torrefaction and pyrolysis. Fuel Process Technol 216:106795

    Article  CAS  Google Scholar 

  • Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Damián AR, Sean MS (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235

    Article  PubMed  Google Scholar 

  • Basalirwa D, Sudo S, Wacal C, Akae F, Oo AZ, Koyama S, Sasagawa D, Yamamoto S, Masunaga T, Nishihara E (2020) Assessment of crop residue and palm shell biochar incorporation on greenhouse gas emissions during the fallow and crop growing seasons of broccoli (Brassica oleracea var. italica). Soil Till Res 196:104435

    Article  Google Scholar 

  • Braker G, Conrad R (2011) Diversity, structure, and size of N2O-producing microbial communities in soils-what matters for their functioning? Adv Appl Microbiol 75:33–70

    Article  CAS  PubMed  Google Scholar 

  • Carter MR, Gregorich EG (2007) Soil sampling and methods of analysis. CRC Press, Boca Ratoon, FL

    Book  Google Scholar 

  • Case SD, Uno H, Nakajima Y, Stoumann JL, Akiyama H, Science S (2018) Bamboo biochar does not affect paddy soil N2O emissions or source following slurry or mineral fertilizer amendment—a 15N tracer study. J Plant Nutr Soil Sc 181:90–98

    Article  CAS  Google Scholar 

  • Chelsea J, Carey N, Dove C, Michael B, Stephen CH, Emma LA (2016) Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea. Soil Biol Biochem 99:158–166

    Article  Google Scholar 

  • Chen H, Li X, Hu F, Shi W (2013) Soil nitrous oxide emissions following crop residue addition: a meta-analysis. Global Change Biol 19:2956–2964

    Article  Google Scholar 

  • Chen H, Liu J, Zhang A, Chen J, Cheng G, Sun B, Pi X, Dyck M, Si B, Zhao Y, Feng H (2017) Effects of straw and plastic film mulching on greenhouse gas emissions in Loess Plateau, China: a field study of 2 consecutive wheat-maize rotation cycles. Sci Total Environ 579:814–824

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Tu X, Meng H, Chen C, Chen Y, Elrys AS, Cheng Y, Zhang J, Cai Z (2021) Microbial process-oriented understanding of stimulation of soil N2O emission following the input of organic materials. Environ Pollut 284:117176

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Zhou W, Luo L, Li Y, Chen Z, Gu Y, Chen Q, Deng O, Xu X, Lan T, Gao X, Zhang S, Deng L (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

    Article  CAS  PubMed  Google Scholar 

  • Chirinda N, Carter MS, Albert KR, Ambus P, Olesen JE, Porter JR, Petersen S (2010) Emissions of nitrous oxide from arable organic and conventional cropping systems on two soil types. Agr Ecosyst Environ 136:199–208

    Article  CAS  Google Scholar 

  • Deng B, Shi Y, Zhang L, Fang H, Gao Y, Luo L, Feng W, Hu X, Wan S, Huang W (2020) Effects of spent mushroom substrate-derived biochar on soil CO2 and N2O emissions depend on pyrolysis temperature. Chemosphere 246:125608

    Article  CAS  PubMed  Google Scholar 

  • Duan P, Zhang X, Zhang Q, Wu Z, Xiong Z (2018) Field-aged biochar stimulated N2O production from greenhouse vegetable production soils by nitrification and denitrification. Sci Total Environ 642:1303–1310

    Article  CAS  PubMed  Google Scholar 

  • Frostegård Å, Vick SH, Lim NY, Bakken LR, Shapleigh J (2022) Linking meta-omics to the kinetics of denitrification intermediates reveals pH-dependent causes of N2O emissions and nitrite accumulation in soil. ISME J 16:26–37

    Article  PubMed  Google Scholar 

  • Gao X, Tang X, Zhao K, Balan V, Zhu Q (2021) Biogas production from anaerobic co-digestion of spent mushroom substrate with different livestock manure. Energies 14:570

    Article  CAS  Google Scholar 

  • Germon M (2008) N2O emission in maize-crops fertilized with pig slurry, matured pig manure or ammonium nitrate in Brittany. Agr Ecosyst Environ 123:201–210

    Article  Google Scholar 

  • Gong F, Sun Y, Wu T, Chen F, Liang B, Wu J (2022) Effects of reducing nitrogen application and adding straw on N2O emission and soil nitrogen leaching of tomato in greenhouse. Chemosphere 301:134549

    Article  CAS  PubMed  Google Scholar 

  • Gu J, Nicoullaud B, Rochette P, Grossel A, Hénault C, Cellier P, Richard G (2013) A regional experiment suggests that soil texture is a major control of N2O emissions from tile-drained winter wheat fields during the fertilization period. Soil Biol Biochem 60:134–141

    Article  CAS  Google Scholar 

  • Harter J, Krause HM, Schuettler S, Ruser R, Fromme M, Scholten T, Kappler A, Behrens S (2014) Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME J 8:660–674

    Article  CAS  PubMed  Google Scholar 

  • Ju X, Xing G, Chen X, Zhang S, Zhang L, Liu X, Cui Z, Yin B, Christie P, Zhu Z (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci USA 106:3041–3046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kabel MA, Jurak E, Mäkelä MR, De Vries R (2017) Occurrence and function of enzymes for lignocellulose degradation in commercial Agaricus bisporus cultivation. Appl Microbiol Biot 101:4363–4369

    Article  CAS  Google Scholar 

  • Keiluweit M, Gee K, Denney A, Fendorf S (2018) Anoxic microsites in upland soils dominantly controlled by clay content. Soil Biol Biochem 118:42–50

    Article  CAS  Google Scholar 

  • Li X, Li Z, Zhang X, Xia L, Zhang W, Ma Q, He H (2020) Disentangling immobilization of nitrate by fungi and bacteria in soil to plant residue amendment. Geoderma 374:114450

    Article  CAS  Google Scholar 

  • Li H, Song X, Bakken LR, Ju X (2023) Reduction of N2O emissions by DMPP depends on interaction of nitrogen source (digestate vs. urea) with soil properties. J Integr Agr 22:251–264

    Article  CAS  Google Scholar 

  • Liu B, Wang X, Ma L, Chadwick D, Chen X (2021) Combined applications of organic and synthetic nitrogen fertilizers for improving crop yield and reducing reactive nitrogen losses from China’s vegetable systems: a meta-analysis. Environ Pollut 269:116143

    Article  CAS  PubMed  Google Scholar 

  • Lou Z, Sun Y, Zhou X, Baig SA, Hu B, Xu X (2017) Composition variability of spent mushroom substrates during continuous cultivation, composting process, and their effects on mineral nitrogen transformation in soil. Geoderma 307:30–37

    Article  CAS  Google Scholar 

  • Martens-Habbena W, BerubeM PM, Urakawa H, Torre JRDL, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979

    Article  CAS  PubMed  Google Scholar 

  • Medina E, Paredes C, Bustamante M, Moral R, Moreno-Caselles J (2012) Relationships between soil physico-chemical, chemical and biological properties in a soil amended with spent mushroom substrate. Geoderma 173:152–161

    Article  Google Scholar 

  • Mei K, Wang Z, Huang H, Zhang C, Shang X, Dahlgren RA, Zhang M, Xia F (2018) Stimulation of N2O emission by conservation tillage management in agricultural lands: a meta-analysis. Soil till Res 182:86–93

    Article  Google Scholar 

  • Meng X, Liu B, Xi C, Luo X, Yuan X, Wang X, Zhu W, Wang H, Cui Z (2018) Effect of pig manure on the chemical composition and microbial diversity during co-composting with spent mushroom substrate and rice husks. Bioresour Technol 251:22–30

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Ma C, Petersen SO (2022) Sensitive control of N2O emissions and microbial community dynamics by organic fertilizer and soil interactions. Biol Fert Soils 58:771–788

    Article  CAS  Google Scholar 

  • Murphy J, Riley J (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Ogbonna D, Ngah S, Okparanma R, Ule O, Nrior R (2020) Percentage bioremediation assessment of spent mushroom substrate (SMS) and mucor racemosus in hydrocarbon contaminated soil. J Adv Microbiology 20:1–21

    Article  Google Scholar 

  • Ohga S, Royse D (2004) Cultivation of Pleurotus eryngii on umbrella plant (Cyperus alternifolius) substrate. J Wood Sci 50:466–469

    Article  Google Scholar 

  • Paredes C, Medina E, Moral R, Pérez-Murcia MD, Moreno-Caselles J, Angeles BM, Cecilia J (2009) Characterization of the different organic matter fractions of spent mushroom substrate. Communi Soil Sci Plan 40:150–161

    Article  CAS  Google Scholar 

  • Paula FS, Tatti E, Abram F, Wilson J, O’Flaherty V (2017) Stabilization of spent mushroom substrate for application as a plant growth-promoting organic amendment. J Environ Manage 196:476–486

    Article  CAS  PubMed  Google Scholar 

  • Pilegaard K (2013) Processes regulating nitric oxide emissions from soils. Philos T R Soc B 368:20130126

    Article  Google Scholar 

  • Pörtner H, Roberts D, Tignor M, Poloczanska E, Mintenbeck K, Alegría A, Craig M, Langsdorf S, Löschke S, Möller V (2022) Climate Change 2022: impacts, adaptation, and vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press: Cambridge, UK

  • Prosser JI, Hink L, Gubry-Rangin C, Nicol G (2020) Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies. Global Change Biol 26:103–118

    Article  Google Scholar 

  • Rajavat AS, Mageshwaran V, Bharadwaj A, Tripathi S, Pandiyan K (2022) Spent mushroom waste: an emerging bio-fertilizer for improving soil health and plant productivity. New Future Dev Microb Biotechnol Bioeng 2:345–354

    Google Scholar 

  • Reay DS, Davidson EA, Smith KA, Smith P, Melillo JM, Dentener F, Crutzen PJ (2012) Global agriculture and nitrous oxide emissions. Nat Clim Change 2:410–416

    Article  CAS  Google Scholar 

  • Rudisill MA, Turco RF, Hoagland L (2016) Fertility practices and rhizosphere effects alter ammonia oxidizer community structure and potential nitrification activity in pepper production soils. App Soil Ecol 99:70–77

    Article  Google Scholar 

  • Senbayram M, Wei Z, Wu D, Shan J, Yan X, Well R (2022) Inhibitory effect of high nitrate on N2O reduction is offset by long moist spells in heavily N loaded arable soils. Biol Fert Soils 58:77–90

    Article  CAS  Google Scholar 

  • Shakoor A, Shakoor S, Rehman A, Ashraf F, Abdullah M, Shahzad SM, Farooq TH, Ashraf M, Manzoor MA, Altaf MM (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

    Article  CAS  Google Scholar 

  • Shi Y, Liu X, Zhang Q, Gao P, Ren J (2019) Sediments. Biochar and organic fertilizer changed the ammonia-oxidizing bacteria and archaea community structure of saline–alkali soil in the North China Plain. J Soil Sediment 20:12–23

    Article  Google Scholar 

  • Stajic M, Vukojevic J, Duletić-Laušević S (2009) Biology of Pleurotus eryngii and role in biotechnological processes: a review. Crit Rev Biotechnol 29:55–66

    Article  CAS  PubMed  Google Scholar 

  • Tao R, Li J, Hu B, Chu G (2021) Mitigating N2O emission by synthetic inhibitors mixed with urea and cattle manure application via inhibiting ammonia-oxidizing bacteria, but not archaea, in a calcareous soil. Environ Pollut 273:116478

    Article  CAS  PubMed  Google Scholar 

  • Tzanakakis VA, Taylor AE, Bakken LR, Bottomley PJ, Myrold DD, Dörsch P (2019) Relative activity of ammonia oxidizing archaea and bacteria determine nitrification dependent N2O emissions in Oregon forest soils. Soil Biol Biochem 139:107612

    Article  CAS  Google Scholar 

  • Vahid Afagh H, Saadatmand S, Riahi H, Khavari-Nejad R, Analysis P (2019) Influence of spent mushroom compost (SMC) as an organic fertilizer on nutrient, growth, yield, and essential oil composition of German chamomile (Matricaria recutita L.). Commun Soil Sci Plant 50:538–548

    Article  CAS  Google Scholar 

  • Valverde ME, Hernández-Pérez T, Paredes-López O (2015) Edible mushrooms: improving human health and promoting quality life. Int J Microbiol 7:376387

    Google Scholar 

  • Vance ED, Brookes PC, Jenkinson D (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Wang J, Chen Z, Xu C, Elrys AS, Shen F, Cheng Y, Chang S (2021) Organic amendment enhanced microbial nitrate immobilization with negligible denitrification nitrogen loss in an upland soil. Environ Pollut 288:117721

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Liang G, Hui D, Deng Q, Xiong X, Qiu Q, Liu J, Chu G, Zhou G, Zhang D (2016) Prolonged acid rain facilitates soil organic carbon accumulation in a mature forest in Southern China. Sci Total Environ 544:94–102

    Article  CAS  PubMed  Google Scholar 

  • Wu W, Lin Z, Zhu X, Li G, Zhang W, Chen Y, Ren L, Luo S, Lin H, Zhou H (2022) Improved tomato yield and quality by altering soil physicochemical properties and nitrification processes in the combined use of organic-inorganic fertilizers. Eur J Soil Biol 109:103384

    Article  CAS  Google Scholar 

  • Xu X, Yuan X, Zhang Q, Wei Q, Liu X, Deng W, Wang J, Yang W, Deng B, Zhang L (2022) Biochar derived from spent mushroom substrate reduced N2O emissions with lower water content but increased CH4 emissions under flooded condition from fertilized soils in Camellia oleifera plantations. Chemosphere 287:132110

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Zhao D, Ma Y, Yang G, Ambus PL, Liu X, Luo J (2023) Effects of long-term organic fertilizer substitutions on soil nitrous oxide emissions and nitrogen cycling gene abundance in a greenhouse vegetable field. Appl Soil Ecol 188:104877

    Article  Google Scholar 

  • Ye G, Lin Y, Kuzyakov Y, Liu D, Luo J, Lindsey S, Wang W, Fan J, Ding W (2019) Manure over crop residues increases soil organic matter but decreases microbial necromass relative contribution in upland Ultisols: Results of a 27-year field experiment. Soil Biol Biochem 134:15–24

    Article  CAS  Google Scholar 

  • Yu H, Ding W, Chen Z, Zhang H, Luo J, Bolan N (2015) Accumulation of organic C components in soil and aggregates. Sci Rep-UK 5:1–12

    Google Scholar 

  • Zhang X, Fang Q, Zhang T, Ma W, Velthof GL, Hou Y, Oenema O, Zhang F (2020) Benefits and trade-offs of replacing synthetic fertilizers by animal manures in crop production in China: a meta-analysis. Global Change Biol 26:888–900

    Article  Google Scholar 

  • Zhang B, Zhou M, Zhu B, Xiao Q, Wang T, Tang J, Yao Z, Kiese R, Butterbach-Bahl K, Brüggemann N (2021a) Soil type affects not only magnitude but also thermal sensitivity of N2O emissions in subtropical mountain area. Sci Total Environ 797:149127

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Penton CR, Yu Z, Xue C, Chen Q, Chen Z, Yan C, Zhang Q, Zhao M, Quensen JF (2021b) A new primer set for Clade I nosZ that recovers genes from a broader range of taxa. Biol Fert Soils 57:523–531

    Article  CAS  Google Scholar 

  • Zhou M, Zhu B, Wang S, Zhu X, Vereecken H, Brüggemann N (2017) Stimulation of N2O emission by manure application to agricultural soils may largely offset carbon benefits: a global meta-analysis. Global Change Biol 23:4068–4083

    Article  Google Scholar 

  • Zhou J, Li B, Xia L, Fan C, Xiong Z (2019) Organic-substitute strategies reduced carbon and reactive nitrogen footprints and gained net ecosystem economic benefit for intensive vegetable production. J Clean Prod 225:984–994

    Article  CAS  Google Scholar 

  • Zou W, Lang M, Zhang L, Liu B, Chen X (2022) Ammonia-oxidizing bacteria rather than ammonia-oxidizing archaea dominate nitrification in a nitrogen-fertilized calcareous soil. Sci Total Environ 811:151402

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported by the National Key Research and Development Program of China (2021YFD1700804-01), the Jiangsu Agriculture Science and Technology Innovation Fund (CX (21) 2024), the Jiangsu Basic Research Program (BK 20230750), and the Jiangsu Excellent Postdoctoral Program (JB 0206025).

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Yang, G., Ma, Y., Xu, W. et al. Spent mushroom substrate as a substitute for chemical fertilizer changes N-cycling genes and reduces N2O emission in different textured soils. Biol Fertil Soils 60, 87–99 (2024). https://doi.org/10.1007/s00374-023-01772-y

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