Abstract
Nitrous oxide (N2O) is a critical greenhouse gas and an ozone-depleting substance, with a global warming potential 298–310 times greater than that of CO2. Mitigating N2O emissions from soils has environmental benefits. Recent research indicates that biochar can serve as an “electron shuttle” to reduce N2O emissions from soils. Electron shuttle is defined as organic molecules capable of reversibly receiving and donating electrons. Thus, biochar is expected to facilitate stepwise reduction of denitrification products, reducing N2O to environmentally harmless N2. However, it remains uncertain whether biochar’s capacity to mitigate N2O can be enlarged by augmenting its function as an electron shuttle. Thus, this study prepared a biochar with enhanced electron shuttle potential by loading redox-active (Fe) onto biochar. The effectiveness of this biochar in mitigating soil N2O emissions was investigated by incorporating it into the soil. The results showed that Fe-loaded biochar significantly augmented its function as an electron shuttle and dramatically reduced soil N2O emissions by 92% compared to the original biochar. The degree of decrease in N2O emissions was strongly associated with both the electron shuttle capacity and the concentration of redox-active Fe in the biochar. Additionally, Fe-loaded biochar significantly decreased the N2O/(N2O + N2) emission ratio and increased the expression of the nosZ-II gene. Our findings suggest that redox-active Fe loading in biochar is an effective strategy to enhance its electron shuttle function. The augmented electron shuttle function of biochar can successfully facilitate N2O mitigation emission by promoting complete denitrification.
Similar content being viewed by others
References
Assessment Report of the Intergovernmental Panel on Climate Change https://doi.org/10.1017/9781009157896
Baggs EM (2011) Soil microbial sources of nitrous oxide: recent advances in knowledge, emerging challenges and future direction. Curr Opin Env Sust 3:321–327. https://doi.org/10.1016/j.cosust.2011.08.011
Brassard P, Godbout S, Palacios JH, Jeanne T, Hogue R, Dubé P, Limousy L, Raghavan V (2018) Effect of six engineered biochars on GHG emissions from two agricultural soils: a short-term incubation study. Geoderma 327:73–84. https://doi.org/10.1016/j.geoderma.2018.04.022
Chacón FJ, Sánchez-Monedero MA, Lezama L, Cayuela ML (2020) Enhancing biochar redox properties through feedstock selection, metal preloading and post-pyrolysis treatments. Chem Eng J 395:125100. https://doi.org/10.1016/j.cej.2020.125100
Chen D, Yang K, Wei L, Wang H (2016) Microbial community and metabolism activity in a bioelectrochemical denitrification system under long-term presence of p-nitrophenol. Bioresour Technol 218:189–195. https://doi.org/10.1016/j.biortech.2016.06.081
Chu D, Dong H, Li Y, Jin Z, Xiao J, Xiang S, Dong Q, Hou X (2022) Enhanced activation of sulfite by a mixture of zero-valent Fe-Mn bimetallic nanoparticles and biochar for degradation of sulfamethazine in water. Sep Purif Technol 285:120315. https://doi.org/10.1016/j.seppur.2021.120315
Chun CL, Baer DR, Matson DW, Amonette JE, Penn RL (2010) Characterization and reactivity of iron nanoparticles prepared with added Cu, pd, and Ni. Environ Sci Technol 44:5079–5085. https://doi.org/10.1021/es903278e
Costa RCC, Lelis MFF, Oliveira LCA, Fabris JD, Ardisson JD, Rios RRVA, Silva CN, Lago RM (2006) Novel active heterogeneous Fenton system based on Fe3 – xMxO4 (Fe, Co, Mn, Ni): the role of M2+ species on the reactivity towards H2O2 reactions. J Hazard Mater 129:171–178. https://doi.org/10.1016/j.jhazmat.2005.08.028
Debasish S, Gobinda GK, Ashutosh KS, Kalyan M (2013) High-performance pseudocapacitor electrodes based on α–Fe2O3/MnO2 core – shell nanowire heterostructure arrays. J Phys Chem C 117:8. https://doi.org/10.1021/jp4039573
Diao ZH, Xu XR, Jiang D, Kong LJ, Sun YX, Hu YX, Hao QW, Chen H (2016) Bentonite-supported nanoscale zero-valent iron/persulfate system for the simultaneous removal of cr(VI) and phenol from aqueous solutions. Chem Eng J 302:213–222. https://doi.org/10.1016/j.cej.2016.05.062
Dorich RA, Nelson DW (1983) Direct colorimetric measurement of ammonium in potassium chloride extracts of soils. Soil Sci Soc Am J 47:833–836. https://doi.org/10.2136/sssaj1983.03615995004700040042x
Forster P, Storelvmo T, Armour K, Collins W, Dufresne JL, Frame D, Lunt DJ, Mauritsen T, Palmer MD, Watanabe M, Wild M, Zhang H (2021) The earth’s energy budget, climate feedbacks, and climate sensitivity. In: Climate Change 2021: the Physical Science Basis. Contribution of Working Group I 40 to the Sixth
Gu H, Gao Y, Xiong M, Zhang D, Chen W, Xu Z (2021) Removal of nitrobenzene from aqueous solution by graphene/biochar supported nanoscale zero-valent-iron: reduction enhancement behavior and mechanism. Sep Purif Technol 275:119146. https://doi.org/10.1016/j.seppur.2021.119146
Haghighi Mood S, Pelaez-Samaniego MR, Garcia-Perez M (2022) Perspectives of engineered biochar for environmental applications: a review. Energ Fuel 36:7940–7986. https://doi.org/10.1021/acs.energyfuels.2c01201
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. https://doi.org/10.1038/ismej.2013.160
Highton MP, Bakken LR, Dörsch P, Tobias-Hunefeldt S, Molstad L, Morales SE (2023) Soil water extract and bacteriome determine N2O emission potential in soils. Biol Fertil Soils 59:217–232. https://doi.org/10.1007/s00374-022-01690-5
Huang B, Yu K, Gambrell RP (2009) Effects of ferric iron reduction and regeneration on nitrous oxide and methane emissions in a rice soil. Chemosphere 74:481–486. https://doi.org/10.1016/j.chemosphere.2008.10.015
Huang BC, Jiang J, Huang GX, Yu HQ (2018) Sludge biochar-based catalysts for improved pollutant degradation by activating peroxymonosulfate. J Mater Chem A 6:8978–8985. https://doi.org/10.1039/C8TA02282H
Ji C, Han Z, Zheng F, Wu S, Wang J, Wang J, Zhang H, Zhang Y, Liu S, Li S, Zou J (2022) Biochar reduced soil nitrous oxide emissions through suppressing fungal denitrification and affecting fungal community assembly in a subtropical tea plantation. Agric Ecosyst Environ 326:107784. https://doi.org/10.1016/j.agee.2021.107784
Jia L, Liu H, Kong Q, Li M, Wu S, Wu H (2020) Interactions of high-rate nitrate reduction and heavy metal mitigation in iron-carbon-based constructed wetlands for purifying contaminated groundwater. Water Res 169:115285. https://doi.org/10.1016/j.watres.2019.115285
Jiang Z, Lv L, Zhang W, Du Q, Pan B, Yang L, Zhang Q (2011) Nitrate reduction using nanosized zero-valent iron supported by polystyrene resins: role of surface functional groups. Water Res 45:2191–2198. https://doi.org/10.1016/j.watres.2011.01.005
Joseph S, Graber ER, Chia C, Munroe P, Donne S, Thomas T, Nielsen S, Marjo C, Rutlidge H, Pan GX, Li L, Taylor P, Rawal A, Hook J (2013) Shifting paradigms: development of high-efficiency biochar fertilizers based on nano-structures and soluble components. Carbon Mana 4:323–343. https://doi.org/10.4155/CMT.13.23
Kammann C, Ippolito J, Hagemann N, Borchard N, Cayuela ML, Estavillo JM, Fuertes-Mendizabal T, Jeffery S, Kern J, Novak J, Rasse D, Saarnio S, Schmidt HP, Spokas K, Wrage-Monnig N (2017) Biochar as a tool to reduce the agricultural greenhouse-gas burden-knowns, unknowns and future research needs. J Environ Eng Landsc 25:114–139. https://doi.org/10.3846/16486897.2017.1319375
Klüpfel L, Keiluweit M, Kleber M, Sander M (2014) Redox properties of plant biomass-derived black carbon (biochar). Environ Sci Technol 48:5601–5611. https://doi.org/10.1021/es500906d
Li S, Shao L, Zhang H, He P, Lu F (2020) Quantifying the contributions of surface area and redox-active moieties to electron exchange capacities of biochar. J Hazard Mater 394:122541. https://doi.org/10.1016/j.jhazmat.2020.122541
Li Z, Sun Y, Yang Y, Han Y, Wang T, Chen J, Tsang DCW (2020b) Biochar-supported nanoscale zero-valent iron as an efficient catalyst for organic degradation in groundwater. J Hazard Mater 383:121240. https://doi.org/10.1016/j.jhazmat.2019.121240
Li X, Qin Y, Jia Y, Li Y, Zhao Y, Pan Y, Sun J (2021) Preparation and application of Fe/biochar (Fe-BC) catalysts in wastewater treatment: a review. Chemosphere 274:129766. https://doi.org/10.1016/j.chemosphere.2021.129766
Li H, Meng J, Liu Z, Lan Y, Yang X, Huang Y, He T, Chen W (2021a) Effects of biochar on N2O emission in denitrification pathway from paddy soil: a drying incubation study. Sci Total Environ 787:147591. https://doi.org/10.1016/j.scitotenv.2021.147591
Liu Y, Wang J (2019) Reduction of nitrate by zero valent iron (ZVI)-based materials: a review. Sci Total Environ 671:388–403. https://doi.org/10.1016/j.scitotenv.2019.03.317
Liu Z, Zhang FS, Wu J (2010) Characterization and application of chars produced from pinewood pyrolysis and hydrothermal treatment. Fuel 89:510–514. https://doi.org/10.1016/j.fuel.2009.08.042
Liu Q, Liu B, Zhang Y, Lin Z, Zhu T, Sun R, Wang X, Ma J, Bei Q, Liu G, Lin X, Xie Z (2017) Can biochar alleviate soil compaction stress on wheat growth and mitigate soil N2O emissions? Soil Biol Biochem 104:8–17. https://doi.org/10.1016/j.soilbio.2016.10.006
Liu Q, Zhang Y, Liu B, Amonette JE, Lin Z, Liu G, Ambus P, Xie Z (2018) How does biochar influence soil N cycle? A meta-analysis. Plant Soil 426:211–225. https://doi.org/10.1007/s11104-018-3619-4
Liu T, Qin S, Pang Y, Yao J, Zhao X, Clough T, Wrage-Mönnig N, Zhou S (2019) Rice root Fe plaque enhances paddy soil N2O emissions via Fe(II) oxidation-coupled denitrification. Soil Biol Biochem 139:107610. https://doi.org/10.1016/j.soilbio.2019.107610
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408. https://doi.org/10.1016/j.fuel.2009.08.042
Logan BE, Rossi R, Ragab Aa, Saikaly PE (2019) Electroactive microorganisms in bioelectrochemical systems. Nat Rev Microbiol 17:307–319. https://doi.org/10.1038/s41579-019-0173-x
Madzaki H, KarimGhani WAWAB, Rebitanim NZ, Alias AB (2016) Carbon dioxide adsorption on sawdust biochar. Procedia Eng 148:718–725. https://doi.org/10.1016/j.proeng.2016.06.591
Mantel S, Dondeyne S, Deckers (2023) World reference base for soil resources (WRB). Goss, Margaret Oliver Encyclopedia of Soils in the Environment, 2nd ed.; Michael, J., Ed, 2023: 206–217. https://doi.org/10.1016/B978-0-12-822974-3.00161-0
Molstad L, Dörsch P, Bakken LR (2007) Robotized incubation system for monitoring gases (O2, NO, N2O, N2) in denitrifying cultures. J Microbiol Methods 71:202–211. https://doi.org/10.1016/j.mimet.2007.08.011
Nelissen V, Saha BK, Ruysschaert G, Boeckx P (2014) Effect of different biochar and fertilizer types on N2O and NO emissions. Soil Biol Biochem 70:244–255. https://doi.org/10.1016/j.soilbio.2013.12.026
Nguyen BT, Lehmann J, Kinyangi J, Smernik R, Riha SJ, Engelhard MH (2009) Long-term black carbon dynamics in cultivated soil. Biogeochemistry 92:163–176. https://doi.org/10.1007/s10533-008-9248-x
Nguyen TTN, Xu CY, Tahmasbian I, Che R, Xu Z, Zhou X, Wallace HM, Bai SH (2017) Effects of biochar on soil available inorganic nitrogen: a review and meta-analysis. Geoderma 288:79–96. https://doi.org/10.1016/j.geoderma.2016.11.004
Norman RJ, Stucki JW (1981) The determination of nitrate and nitrite in soil extracts by ultraviolet spectrophotometry. Soil Sci Soc Am J 45:347–353. https://doi.org/10.2136/sssaj1981.03615995004500020024x
Norman RJ, Edberg JC, Stucki JW (1985) Determination of nitrate in soil extracts by dual-wavelength ultraviolet spectrophotometry. Soil Sci Soc Am J 49:1182–1185. https://doi.org/10.2136/sssaj1985.03615995004900050022x
Obia A, Cornelissen G, Mulder J, Dörsch P (2015) Effect of soil pH increase by biochar on NO, N2O and N2 production during denitrification in acid soils. PLoS ONE 10:e0138781. https://doi.org/10.1371/journal.pone.0138781
Oh SY, Son JG, Chiu PC (2013) Biochar-mediated reductive transformation of nitro herbicides and explosives. Environ Toxicol Chem 32:501–508. https://doi.org/10.1002/etc.2087
Qin S, Wang Y, Hu C, Oenema O, Li X, Zhang Y, Dong W (2012) Yield-scaled N2O emissions in a winter wheat–summer corn double-cropping system. Atmos Environ 55:240–244. https://doi.org/10.1016/j.atmosenv.2012.02.077
Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125. https://doi.org/10.1126/science.1176985
Ruan X, Sun Y, Du W, Tang Y, Liu Q, Zhang Z, Doherty W, Frost RL, Qian G, Tsang DCW (2019) Formation, characteristics, and applications of environmentally persistent free radicals in biochars: a review. Bioresour Technol 281:457–468. https://doi.org/10.1016/j.biortech.2019.02.105
Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-García C, Rodríguez G, Massol-Deyá A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Löffler FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. PNAS 109:19709–19714. https://doi.org/10.1073/pnas.1211238109
Saquing JM, Yu YH, Chiu PC (2016) Wood-derived black carbon (biochar) as a microbial electron donor and acceptor. Environ Sci Technol Lett 3:62–66. https://doi.org/10.1021/acs.estlett.5b00354
Semedo M, Song B, Sparrer T, Phillips RL (2018) Antibiotic effects on microbial communities responsible for denitrification and N2O production in grassland soils. Fronti Microbiol 9:10. https://doi.org/3389/fmicb.2018.02121
Shen Y, Zhuang L, Zhang J, Fan J, Yang T, Sun S (2019) A study of ferric-carbon micro-electrolysis process to enhance nitrogen and phosphorus removal efficiency in subsurface flow constructed wetlands. Chem Eng J 359:706–712. https://doi.org/10.1016/j.cej.2018.11.152
Shen W, Xue H, Gao N, Shiratori Y, Kamiya T, Fujiwara T, Isobe K, Senoo K (2020) Effects of copper on nitrous oxide (N2O) reduction in denitrifiers and N2O emissions from agricultural soils. Biol Fertil Soils 56:39–51. https://doi.org/10.1007/s00374-019-01399-y
Shi RY, Ni N, Nkoh JN, Li JY, Xu RK, Qian W (2019) Beneficial dual role of biochars in inhibiting soil acidification resulting from nitrification. Chemosphere 234:43–51. https://doi.org/10.1016/j.chemosphere.2019.06.030
Sun T, Levin BD, Guzman JJ, Enders A, Muller DA, Angenent LT, Lehmann J (2017) Rapid electron transfer by the carbon matrix in natural pyrogenic carbon. Nat Commun 8:14873. https://doi.org/10.1038/ncomms14873
Sun X, Yang J, Jiang H, Wang B, Xiao H, Xie Z, Han J, Zhang X, Xu J, Gong D, Zhang X, Wang Y (2022) Nitrite- and N2O-reducing bacteria respond differently to ecological factors in saline lakes. https://doi.org/10.1093/femsec/fiac007. FEMS Microbiol Ecol
Van der Zee FP, Cervantes FJ (2009) Impact and application of electron shuttles on the redox (bio) transformation of contaminants: a review. Biotechnol Adv 27:256–277. https://doi.org/10.1016/j.biotechadv.2009.01.004
Wan Z, Sun Y, Tsang DCW, Hou D, Cao X, Zhang S, Gao B, Ok YS (2020) Sustainable remediation with an electroactive biochar system: mechanisms and perspectives. Green Chem 22:2688–2711. https://doi.org/10.1039/D0GC00717J
Wang X, Du Y, Ma J (2016) Novel synthesis of carbon spheres supported nanoscale zero-valent iron for removal of metronidazole. Appl Surf Sci 390:50–59. https://doi.org/10.1016/j.apsusc.2016.08.027
Xu J, Che P, Ma Y (1996) More sensitive way to determine iron using an iron(II) – 1, 10-phenanthroline complex and capillary electrophoresis. J Chromatogr 749:287–294. https://doi.org/10.1016/0021-9673(96)00457-8
Xu HJ, Wang XH, Li H, Yao HY, Su JQ, Zhu YG (2014) Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environ Sci Technol 48:9391–9399. https://doi.org/10.1021/es5021058
Xu X, Xu Z, Huang J, Gao B, Zhao L, Qiu H, Cao X (2021) Sorption of reactive red by biochars ball milled in different atmospheres: co-effect of surface morphology and functional groups. Chem Eng J 413:127468. https://doi.org/10.1016/j.cej.2020.127468
Xu Z, Wan Z, Sun Y, Gao B, Hou D, Cao X, Komarek M, Ok YS, Tsang DCW (2022) Electroactive Fe-biochar for redox-related remediation of arsenic and chromium: distinct redox nature with varying iron/carbon speciation. J Hazard Mater 430:128479. https://doi.org/10.1016/j.jhazmat.2022.128479
Yan Q, Wan C, Liu J, Gao J, Yu F, Zhang J, Cai Z (2013) Iron nanoparticles in situ encapsulated in biochar-based carbon as an effective catalyst for the conversion of biomass-derived syngas to liquid hydrocarbons. Green Chem 15:1631–1640. https://doi.org/10.1039/C3GC37107G
Yang F, Zhao L, Gao B, Xu X, Cao X (2016) The interfacial behavior between biochar and soil minerals and its effect on biochar stability. Environ Sci Technol 50:2264–2271. https://doi.org/10.1021/acs.est.5b03656
Yu Z, Tang J, Liao H, Liu X, Zhou P, Chen Z, Rensing C, Zhou S (2018) The distinctive microbial community improves composting efficiency in a full-scale hyperthermophilic composting plant. Bioresour Technol 265:146–154. https://doi.org/10.1016/j.biortech.2018.06.011
Yu W, Chu C, Chen B (2022) Enhanced microbial ferrihydrite reduction by pyrogenic carbon: impact of graphitic structures. Environ Sci Technol 56:239–250. https://doi.org/10.1021/acs.est.1c04440
Yuan H, Lu T, Wang Y, Huang H, Chen Y (2014) Influence of pyrolysis temperature and holding time on properties of biochar derived from medicinal herb (radix isatidis) residue and its effect on soil CO2 emission. J Anal Appl Pyrol 110:277–284. https://doi.org/10.1016/j.jaap.2014.09.016
Yuan Y, Bolan N, Prevoteau A, Vithanage M, Biswas JK, Ok YS, Wang H (2017) Applications of biochar in redox-mediated reactions. Bioresour Technol 246:271–281. https://doi.org/10.1016/j.biortech.2017.06.154
Yuan H, Zhang Z, Li M, Clough T, Wrage-Mönnig N, Qin S, Ge T, Liao H, Zhou S (2019) Biochar’s role as an electron shuttle for mediating soil N2O emissions. Soil Biol Biochem 133:94–96. https://doi.org/10.1016/j.soilbio.2019.03.002
Yuan H, Zeng J, Yuan D, Zhang L, Qin S, Wrage-Mönnig N, Clough T, Zhou S (2020) Co-application of a biochar and an electric potential accelerates soil nitrate removal while decreasing N2O emission. Soil Biol Biochem 149:107946. https://doi.org/10.1016/j.soilbio.2020.107946
Yuan D, Yuan H, He X, Hu H, Qin S, Clough T, Wrage-Mönnig N, Luo J, He X, Chen M, Zhou S (2021) Identification and verification of key functional groups of biochar influencing soil N2O emission. Biol Fertil Soils 57:447–456. https://doi.org/10.1007/s00374-021-01541-9
Yuan J, Wen Y, Dionysiou DD, Sharma VK, Ma X (2022) Biochar as a novel carbon-negative electron source and mediator: electron exchange capacity (EEC) and environmentally persistent free radicals (EPFRs): a review. Chem Eng J 429:132313. https://doi.org/10.1016/j.cej.2021.132313
Zhang L, Jiang M, Ding K, Zhou S (2019) Iron oxides affect denitrifying bacterial communities with the nirS and nirK genes and potential N2O emission rates from paddy soil. Eur J Soil Biol 93:103093. https://doi.org/10.1016/j.ejsobi.2019.103093
Zhao Z, Cao Y, Li S, Zhang Y (2021) Effects of biowaste-derived biochar on the electron transport efficiency during anaerobic acid orange 7 removal. Bioresour Technol 320:124295. https://doi.org/10.1016/j.biortech.2020.124295
Acknowledgements
This work was supported by the National Key R&D Program of China (no. 2021YFD1500400), the Natural Science Foundation of Hebei Province (no. D2022503014), the National Natural Science Foundation of China (no. 42277360), and the National Key Research and Development Program of China (no. 2023YFC3707400).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yuan, D., Wu, P., Yuan, J. et al. Loading of redox-active metal Fe largely enhances the capacity of biochar to mitigate soil N2O emissions by promoting complete denitrification. Biol Fertil Soils (2024). https://doi.org/10.1007/s00374-024-01823-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00374-024-01823-y