Biochar-microplastics interaction modulates soil nitrous oxide emissions and microbial communities

Ziheng Zou , Qidong Yu , Runyu Chen , Jinyang Wang , Xueyan Liu

Biochar ›› 2025, Vol. 7 ›› Issue (1) : 15

PDF
Biochar ›› 2025, Vol. 7 ›› Issue (1) : 15 DOI: 10.1007/s42773-024-00413-3
Original Research

Biochar-microplastics interaction modulates soil nitrous oxide emissions and microbial communities

Author information +
History +
PDF

Abstract

Biochar has been proposed as a soil amendment in vegetable fields, where the widespread use of plastic film leads to significant retention of microplastics (MPs) in the soil. However, the interactive effect of biochar and MPs on plant growth and soil functions remains poorly understood. Here, we conducted a pot experiment to examine the effects of biochar application in the presence of conventional and biodegradable microplastics (0.05% w/w) on the growth of coriander, soil nitrogen (N) cycling processes, and microbial communities. The results showed that biochar application increased aboveground biomass by increasing plant available N of NH4 +, regardless of the presence of MPs. Biochar also significantly reduced soil nitrous oxide (N2O) emissions by an average of 16% without MPs. However, when MPs were present, the effect of biochar on N2O emissions was lessened depending on the MP type. Polylactic acid consistently reduced soil N2O emissions and the abundance of N2O production genes, irrespective of biochar application. Conversely, polyethylene without biochar reduced N2O emissions primarily by inhibiting N-related functional genes responsible for nitrification and denitrification. This inhibitory effect was reversed when biochar was applied, leading to a 26% increase in N2O emissions due to increased nifH and nirK gene abundance. Although biochar and MPs did not significantly alter microbial α-diversity, they altered the composition and structure of bacterial and fungal communities, linked to changes in soil N turnover. Our study underscores the critical role of MP type in assessing the effects of biochar on soil N cycling and N2O emissions. Consequently, plastic pollution may complicate the ability of biochar to improve plant growth and soil functions, depending on the characteristics of the MPs.

Cite this article

Download citation ▾
Ziheng Zou, Qidong Yu, Runyu Chen, Jinyang Wang, Xueyan Liu. Biochar-microplastics interaction modulates soil nitrous oxide emissions and microbial communities. Biochar, 2025, 7(1): 15 DOI:10.1007/s42773-024-00413-3

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Baho DL, Bundschuh M, Futter MN. Microplastics in terrestrial ecosystems: moving beyond the state of the art to minimize the risk of ecological surprise. Glob Change Biol, 2021, 27: 3969-3986

[2]

Benbi DK, Brar K. Pyrogenic conversion of rice straw and wood to biochar increases aromaticity and carbon accumulation in soil. Carbon Management, 2021, 12: 385-397

[3]

Bonanomi G, Ippolito F, Cesarano G, Nanni B, Lombardi N, Rita A, Saracino A, Scala F. Biochar as plant growth promoter: better off alone or mixed with organic amendments?. Front Plant Sci, 2017, 8: 1570

[4]

Boots B, Russell CW, Green DS. Effects of microplastics in soil ecosystems: above and below ground. Environ Sci Technol, 2019, 53: 11496-11506

[5]

Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls?. Philos Trans R Soc B Biol Sci, 2013, 368: 20130122

[6]

Cameron KC, Di HJ, Moir JL. Nitrogen losses from the soil/plant system: a review. Ann Appl Biol, 2013, 162: 145-173

[7]

Campbell TP, Ulrich DEM, Toyoda J, Thompson J, Munsky B, Albright MBN, Bailey VL, Tfaily MM, Dunbar J. Microbial communities influence soil dissolved organic carbon concentration by altering metabolite composition. Front Microbiol, 2021, 12 799014

[8]

Castellini M, Giglio L, Niedda M, Palumbo AD, Ventrella D. Impact of biochar addition on the physical and hydraulic properties of a clay soil. Soil Tillage Res, 2015, 154: 1-13

[9]

Cayuela ML, Sanchez-Monedero MA, Roig A, Hanley K, Enders A, Lehmann J. Biochar and denitrification in soils: when, how much and why does biochar reduce N(2)O emissions?. Sci Rep, 2013, 3: 1732

[10]

Chai B, Yin H, Xiao T, Xiao E, Dang Z, Pan K. Effects of microplastics on endophytes in different niches of Chinese flowering cabbage (Brassica campestris). J Agric Food Chem, 2024, 72: 4679-4688

[11]

Chen C, Pan J, Xiao S, Wang J, Gong X, Yin G, Hou L, Liu M, Zheng Y. Microplastics alter nitrous oxide production and pathways through affecting microbiome in estuarine sediments. Water Res, 2022, 221 118733

[12]

Chen Y, Li Y, Liang X, Lu S, Ren J, Zhang Y, Han Z, Gao B, Sun K. Effects of microplastics on soil carbon pool and terrestrial plant performance. Carbon Res, 2024

[13]

Clayton H, Arah JRM, Smith KA. Measurement of nitrous oxide emission from fertilized grassland using micrometeorological techniques. J Geophys Res Atmos, 1994, 99: 16599-16607

[14]

Crouzet O, Consentino L, Pétraud J-P, Marrauld C, Aguer J-P, Bureau S, Le Bourvellec C, Touloumet L, Bérard A. Soil photosynthetic microbial communities mediate aggregate stability: influence of cropping systems and herbicide use in an agricultural soil. Front Microbiol, 2019

[15]

de Klein C, Harvey M. Nitrous oxide chamber methodology guidelines, 2012 Ministry for Primary Industries

[16]

de Souza Machado AA, Lau CW, Kloas W, Bergmann J, Bachelier JB, Faltin E, Becker R, Gorlich AS, Rillig MC. Microplastics can change soil properties and affect plant performance. Environ Sci Technol, 2019, 53: 6044-6052

[17]

De la Rosa JM, Miller AZ, Knicker H. Soil-borne fungi challenge the concept of long-term biochemical recalcitrance of pyrochar. Sci Rep, 2018, 8: 2896

[18]

Fan P, Yu H, Xi B, Tan W. A review on the occurrence and influence of biodegradable microplastics in soil ecosystems: are biodegradable plastics substitute or threat?. Environ Int, 2022, 163 107244

[19]

Fei Y, Huang S, Zhang H, Tong Y, Wen D, Xia X, Wang H, Luo Y, Barcelo D. Response of soil enzyme activities and bacterial communities to the accumulation of microplastics in an acid cropped soil. Sci Total Environ, 2020, 707 135634

[20]

Feng Y, Han L, Sun H, Zhu D, Xue L, Jiang ZT, Poinern GEJ, Lu Q, Feng Y, Xing B. Every coin has two sides: Continuous and substantial reduction of ammonia volatilization under the coexistence of microplastics and biochar in an annual observation of rice-wheat rotation system. Sci Total Environ, 2022, 847 157635

[21]

Firestone MK, Davidson EA. Microbiological basis of NO and N 2 O production and consumption in soil. Exchange Trace Gases between Terrestrial Ecosyst Atmos, 1989, 47: 7-21

[22]

Gao B, Yao H, Li Y, Zhu Y. Microplastic addition alters the microbial community structure and stimulates soil carbon dioxide emissions in vegetable-growing soil. Environ Toxicol Chem, 2021, 40: 352-365

[23]

Gaylarde CC, de Almeida MP, Neves CV, Neto JAB, da Fonseca EM. The importance of biofilms on microplastic particles in their sinking behavior and the transfer of invasive organisms between ecosystems. Micro, 2023, 3: 320-337

[24]

Ge J, Li H, Liu P, Zhang Z, Ouyang Z, Guo X. Review of the toxic effect of microplastics on terrestrial and aquatic plants. Sci Total Environ, 2021, 791 148333

[25]

Greenfield LM, Graf M, Rengaraj S, Bargiela R, Williams G, Golyshin PN, Chadwick DR, Jones DL. Field response of N2O emissions, microbial communities, soil biochemical processes and winter barley growth to the addition of conventional and biodegradable microplastics. Agricult Ecosyst Environ, 2022

[26]

Guo QQ, Xiao MR, Ma Y, Niu H, Zhang GS. Polyester microfiber and natural organic matter impact microbial communities, carbon-degraded enzymes, and carbon accumulation in a clayey soil. J Hazard Mater, 2021, 405 124701

[27]

Han L, Chen L, Li D, Ji Y, Feng Y, Feng Y, Yang Z. Influence of polyethylene terephthalate microplastic and biochar co-existence on paddy soil bacterial community structure and greenhouse gas emission. Environ Pollut, 2022, 292 118386

[28]

Han Y, Teng Y, Wang X, Wen D, Gao P, Yan D, Yang N. Biodegradable PBAT microplastics adversely affect pakchoi (Brassica chinensis L.) growth and the rhizosphere ecology: focusing on rhizosphere microbial community composition, element metabolic potential, and root exudates. Sci Total Environ, 2024, 912 169048

[29]

Hart SC, Stark JM, Davidson EA, Firestone MK, Weaver RW, Peter SA, Bezdicek BD, Ali SS, Wollum TA (1994) Methods of Soil Analysis Part 2 Microbiological and Biochemical Properties. In: Nitrogen mineralization immobilization and nitrification soil science society of America. Madison WI, USA, pp 985-1018

[30]

Hayward MK, Dewey ED, Shaffer KN, Huntington AM, Burchell BM, Stokes LM, Alexander BC, George JE, Kempher ML, Joye SB, Madigan MT (2021) Cultivation and characterization of snowbound microorganisms from the South Pole. Extremophiles 25:159-172. https://doi.org/10.1007/s00792-021-01218-z

[31]

Hernandez-Arenas R, Beltran-Sanahuja A, Navarro-Quirant P, Sanz-Lazaro C. A review ofmicroplastics pollution in the soil and terrestrial ecosystems: a global and Bangladesh perspective. Environ Pollut, 2021, 268 115779

[32]

Hu X, Gu H, Sun X, Wang Y, Liu J, Yu Z, Li Y, Jin J, Wang G. Distinct influence of conventional and biodegradable microplastics on microbe-driving nitrogen cycling processes in soils and plastispheres as evaluated by metagenomic analysis. J Hazard Mater, 2023

[33]

Huang Y, Zhao Y, Wang J, Zhang M, Jia W, Qin X. LDPE microplastic films alter microbial community composition and enzymatic activities in soil. Environ Pollut, 2019, 254 112983

[34]

Joseph S, Cowie AL, Van Zwieten L, Bolan N, Budai A, Buss W, Cayuela ML, Graber ER, Ippolito JA, Kuzyakov Y, et al.. How biochar works, and when it doesn’t: a review of mechanisms controlling soil and plant responses to biochar. Glob Change Biol Bioenergy, 2021, 13: 1731-1764

[35]

Judy JD, Williams M, Gregg A, Oliver D, Kumar A, Kookana R, Kirby JK. Microplastics in municipal mixed-waste organic outputs induce minimal short to long-term toxicity in key terrestrial biota. Environ Pollut, 2019, 252: 522-531

[36]

Khalid N, Aqeel M, Noman A. Microplastics could be a threat to plants in terrestrial systems directly or indirectly. Environ Pollut, 2020, 267 115653

[37]

Khalid AR, Shah T, Asad M, Ali A, Samee E, Adnan F, Bhatti MF, Marhan S, Kammann CI, Haider G. Biochar alleviated the toxic effects of PVC microplastic in a soil-plant system by upregulating soil enzyme activities and microbial abundance. Environ Pollut, 2023, 332 121810

[38]

Khan KY, Tang Y, Cheng P, Song Y, Li X, Lou J, Iqbal B, Zhao X, Hameed R, Li G, Du D. Effects of degradable and non-degradable microplastics and oxytetracycline co-exposure on soil N2O and CO2 emissions. Appl Soil Ecol, 2024

[39]

Klotz MG, Schmid MC, Strous M, Op Den Camp HJ, Jetten MS, Hooper AB (2008) Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ Microbiol 10(11):3150-3163. https://doi.org/10.1111/j.1462-2920.2008.01733.x

[40]

Lefcheck JS, Freckleton R. piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol, 2015, 7: 573-579

[41]

Li HZ, Zhu D, Lindhardt JH, Lin SM, Ke X, Cui L. Long-term fertilization history alters effects of microplastics on soil properties, microbial communities, and functions in diverse farmland ecosystem. Environ Sci Technol, 2021, 55: 4658-4668

[42]

Li X, Yao S, Wang Z, Jiang X, Song Y, Chang SX. Microplastic and biochar coexistence decreases their stimulation on global warming potential resulting from soil greenhouse gas emissions. SSRN Electr J, 2022

[43]

Li X, Yao S, Wang Z, Jiang X, Song Y, Chang SX. Polyethylene microplastic and biochar interactively affect the global warming potential of soil greenhouse gas emissions. Environ Pollut, 2022, 315 120433

[44]

Lian Y, Shi R, Liu J, Zeb A, Wang Q, Wang J, Yu M, Li J, Zheng Z, Ali N, et al.. Effects of polystyrene, polyethylene, and polypropylene microplastics on the soil-rhizosphere-plant system: phytotoxicity, enzyme activity, and microbial community. J Hazard Mater, 2024, 465 133417

[45]

Liu Y, Xu F, Ding L, Zhang G, Bai B, Han Y, Xiao L, Song Y, Li Y, Wan S, Li G. Microplastics reduce nitrogen uptake in peanut plants by damaging root cells and impairing soil nitrogen cycling. J Hazard Mater, 2023, 443 130384

[46]

Lozano YM, Aguilar-Trigueros CA, Onandia G, Maaß S, Zhao T, Rillig MC, Macinnis-Ng C. Effects of microplastics and drought on soil ecosystem functions and multifunctionality. J Appl Ecol, 2021, 58: 988-996

[47]

Lozano YM, Lehnert T, Linck LT, Lehmann A, Rillig MC. Microplastic shape, polymer type, and concentration affect soil properties and plant biomass. Front Plant Sci, 2021, 12 616645

[48]

Lv S, Li Y, Zhao S, Shao Z (2024) Biodegradation of typical plastics: from microbial diversity to metabolic mechanisms. Int J Mol Sci 25(1):593. https://doi.org/10.3390/ijms25010593

[49]

Ma J, Sheng GD, O'Connor P. Microplastics combined with tetracycline in soils facilitate the formation of antibiotic resistance in the Enchytraeus crypticus microbiome. Environ Pollut, 2020, 264 114689

[50]

Meng F, Yang X, Riksen M, Xu M, Geissen V. Response of common bean (Phaseolus vulgaris L.) growth to soil contaminated with microplastics. Sci Total Environ, 2021, 755 142516

[51]

Meng F, Harkes P, van Steenbrugge JJM, Geissen V. Effects of microplastics on common bean rhizosphere bacterial communities. Appl Soil Ecol, 2023

[52]

Miao J, Chen Y, Zhang E, Yang Y, Sun K, Gao B. Effects of microplastics and biochar on soil cadmium availability and wheat plant performance. GCB Bioenergy, 2023, 15: 1046-1057

[53]

Moshood TD, Nawanir G, Mahmud F, Mohamad F, Ahmad MH, AbdulGhani A. Sustainability of biodegradable plastics: new problem or solution to solve the global plastic pollution?. Curr Res Green Sustain Chem, 2022

[54]

Ng EL, Lin SY, Dungan AM, Colwell JM, Ede S, Huerta Lwanga E, Meng K, Geissen V, Blackall LL, Chen D. Microplastic pollution alters forest soil microbiome. J Hazard Mater, 2021, 409 124606

[55]

Norton JM, Stark JM (2011) Regulation and measurement of nitrification in terrestrial systems. Methods Enzymol 486:343–368

[56]

Novair SB, Cheraghi M, Faramarzi F, Lajayer BA, Senapathi V, Astatkie T, Price G. Reviewing the role of biochar in paddy soils: an agricultural and environmental perspective. Ecotoxicol Environ Saf, 2023, 263 115228

[57]

OECD. Global plastics outlook: policy scenarios to 2060 (OECD), 2022 OECD

[58]

Palansooriya KN, Sang MK, El-Naggar A, Shi L, Chang SX, Sung J, Zhang W, Ok YS. Low-density polyethylene microplastics alter chemical properties and microbial communities in agricultural soil. Sci Rep, 2023, 13: 16276

[59]

Pignattelli S, Broccoli A, Piccardo M, Terlizzi A, Renzi M. Effects of polyethylene terephthalate (PET) microplastics and acid rain on physiology and growth of Lepidium sativum. Environ Pollut, 2021, 282 116997

[60]

Qi Y, Yang X, Pelaez AM, Huerta Lwanga E, Beriot N, Gertsen H, Garbeva P, Geissen V. Macro- and micro- plastics in soil-plant system: effects of plastic mulch film residues on wheat (Triticum aestivum) growth. Sci Total Environ, 2018, 645: 1048-1056

[61]

Ran T, Liao H, Zhao Y, Li J. Soil plastisphere interferes with soil bacterial community and their functions in the rhizosphere of pepper (Capsicum annuum L.). Ecotoxicol Environ Saf, 2024, 270 115946

[62]

Ren X, Tang J, Liu X, Liu Q. Effects of microplastics on greenhouse gas emissions and the microbial community in fertilized soil. Environ Pollut, 2020, 256 113347

[63]

Rillig MC, de Souza Machado AA, Lehmann A, Klumper U. Evolutionary implications of microplastics for soil biota. Environ Chem, 2019, 16: 3-7

[64]

Rillig MC, Hoffmann M, Lehmann A, Liang Y, Lück M, Augustin J. Microplastic fibers affect dynamics and intensity of CO2 and N2O fluxes from soil differently. Microplast Nanoplast, 2021

[65]

Seeley ME, Song B, Passie R, Hale RC. Microplastics affect sedimentary microbial communities and nitrogen cycling. Nat Commun, 2020, 11: 2372

[66]

Serrano-Ruiz H, Martin-Closas L, Pelacho AM. Biodegradable plastic mulches: impact on the agricultural biotic environment. Sci Total Environ, 2021, 750 141228

[67]

Shen H, Sun Y, Duan H, Ye J, Zhou A, Meng H, Zhu F, He H, Gu C. Effect of PVC microplastics on soil microbial community and nitrogen availability under laboratory-controlled and field-relevant temperatures. Appl Soil Ecol, 2023

[68]

Sheng Y, Zhu L. Biochar alters microbial community and carbon sequestration potential across different soil pH. Sci Total Environ, 2018, 622–623: 1391-1399

[69]

Sheng Y, Zhan Y, Zhu L. Reduced carbon sequestration potential of biochar in acidic soil. Sci Total Environ, 2016, 572: 129-137

[70]

Stein LY (2011) Surveying N2O-producing pathways in bacteria. Methods Enzymol 486:131–152

[71]

Su P, Gao C, Zhang X, Zhang D, Liu X, Xiang T, Luo Y, Chu K, Zhang G, Bu N, Li Z. Microplastics stimulated nitrous oxide emissions primarily through denitrification: a meta-analysis. J Hazard Mater, 2023, 445 130500

[72]

Tanure MMC, da Costa LM, Huiz HA, Fernandes RBA, Cecon PR, Pereira Junior JD, da Luz JMR. Soil water retention, physiological characteristics, and growth of maize plants in response to biochar application to soil. Soil Tillage Res, 2019, 192: 164-173

[73]

Trivedi AK, Gupta MK, Singh H. PLA based biocomposites for sustainable products: a review. Adv Ind Eng Polym Res, 2023

[74]

UNEP (2022) Historic day in the campaign to beat plastic pollution: nations commit to develop a legally binding agreement. https://www.unep.org/news-and-stories/press-release/historic-day-campaign-beat-plastic-pollution-nations-commit-develop.

[75]

Wang W, Ge J, Yu X, Li H. Environmental fate and impacts of microplastics in soil ecosystems: progress and perspective. Sci Total Environ, 2020

[76]

Wang F, Wang Q, Adams CA, Sun Y, Zhang S. Effects of microplastics on soil properties: current knowledge and future perspectives. J Hazard Mater, 2022, 424 127531

[77]

Wang Q, Feng X, Liu Y, Li W, Cui W, Sun Y, Zhang S, Wang F, Xing B. Response of peanut plant and soil N-fixing bacterial communities to conventional and biodegradable microplastics. J Hazard Mater, 2023, 459 132142

[78]

Wang W, Zhang Z, Gao J, Wu H. The impacts of microplastics on the cycling of carbon and nitrogen in terrestrial soil ecosystems: progress and prospects. Sci Total Environ, 2024, 915 169977

[79]

Wu S, Zhuang G, Bai Z, Cen Y, Xu S, Sun H, Han X, Zhuang X. Mitigation of nitrous oxide emissions from acidic soils by Bacillus amyloliquefaciens, a plant growth-promoting bacterium. Glob Change Biol, 2018, 24: 2352-2365

[80]

Xiao X, Chen Z, Chen B. H/C atomic ratio as a smart linkage between pyrolytic temperatures, aromatic clusters and sorption properties of biochars derived from diverse precursory materials. Sci Rep, 2016, 6: 22644

[81]

Yang F, Wang C, Sun H. A comprehensive review of biochar-derived dissolved matters in biochar application: production, characteristics, and potential environmental effects and mechanisms. J Environ Chem Eng, 2021, 9 105258

[82]

Yang Y, Sun K, Han L, Chen Y, Liu J, Xing B. Biochar stability and impact on soil organic carbon mineralization depend on biochar processing, aging and soil clay content. Soil Biol Biochem, 2022

[83]

Yang X, Wen P, Yang Y, Jia P, Li W, Pei D (2023) Plastic biodegradation by in vitro environmental microorganisms and in vivo gut microorganisms of insects. Front Microbiol 13:1001750

[84]

Yu Y, Li X, Feng Z, Xiao M, Ge T, Li Y, Yao H. Polyethylene microplastics alter the microbial functional gene abundances and increase nitrous oxide emissions from paddy soils. J Hazard Mater, 2022, 432 128721

[85]

Yu Y, Li X, Fan H, Li Y, Yao H. Dose effect of polyethylene microplastics on nitrous oxide emissions from paddy soils cultivated for different periods. J Hazard Mater, 2023, 453 131445

[86]

Zhang S, Pei L, Zhao Y, Shan J, Zheng X, Xu G, Sun Y, Wang F. Effects of microplastics and nitrogen deposition on soil multifunctionality, particularly C and N cycling. J Hazard Mater, 2023, 451 131152

[87]

Zheng J, Chen J, Pan G, Liu X, Zhang X, Li L, Bian R, Cheng K, Jinwei Z. Biochar decreased microbial metabolic quotient and shifted community composition four years after a single incorporation in a slightly acid rice paddy from southwest China. Sci Total Environ, 2016, 571: 206-217

[88]

Zheng B, Zhu Y, Sardans J, Penuelas J, Su J. QMEC: a tool for high-throughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Sci China Life Sci, 2018, 61: 1451-1462

[89]

Zhou J, Gui H, Banfield CC, Wen Y, Zang H, Dippold MA, Charlton A, Jones DL. The microplastisphere: Biodegradable microplastics addition alters soil microbial community structure and function. Soil Biol Biochem, 2021

[90]

Zhu X, Mao L, Chen B. Driving forces linking microbial community structure and functions to enhanced carbon stability in biochar-amended soil. Environ Int, 2019, 133 105211

[91]

Zimmerman AR, Gao B, Ahn M-Y. Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils. Soil Biol Biochem, 2011, 43: 1169-1179

Funding

Startup Foundation for Introducing Talent of Nanjing Agricultural University(030/804028)

RIGHTS & PERMISSIONS

The Author(s)

AI Summary AI Mindmap
PDF

394

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/