Geoconductor function of graphitized biochar redirects microbial Fe(III) reduction and stimulates hydroxyl radical production in paddy soil

Abstract

Integrating biochar into paddy soil as a hybrid geobattery–geoconductor material offers a transformative approach for sustainable soil decontamination. However, biochar often has an undeveloped graphitized structure and poor geoconductor function, restricting the electron transfer capacity for microbial Fe(III) reduction and subsequent •OH generation. In this study, the flash Joule heating method was used to enhance the graphitized structure of biochar to redirect microbial Fe(III) reduction via a geoconductor function-induced electron self-adaptation pathway. Specifically, a highly conductive framework of graphitized biochar (G-biochar) with a 2.64-fold enhancement in electrical conductivity unchoked the electron transfer obstacle between Fe(III)-reducing bacteria (Bacillus, Anaeromyxobacter, Citrifermentans, and Flavisolibacter) and Fe(III), This mechanistic improvement resulted in 18.9% increase in active Fe(II) generation. Accordingly, 54.9% increase in •OH production and 57.2% increase in the sulfamethoxazole degradation rate were evidenced. Finally, G-biochar differentially promoted microbial Fe(III) reduction in various paddy soils, which mainly depended on the activity of the reducing microbial community. These findings redefine the biochar trade-off effect on soil microbial–geochemical processes via the geoconductor function rather than the previously acknowledged geobattery electron reservoir mixing strategy.

Graphical Abstract

Keywords

Biochar / Electron transfer / Geoconductor / Soil microbial Fe(III) reduction / Hydroxyl radicals

References

[1] Barbhuiya NH, Kumar A, Singh A, Chandel MK, Arnusch CJ, Tour JM, Singh SP. The future of flash graphene for the sustainable management of solid waste. ACS Nano, 2021, 15: 15461-15470

[2] Chen N, Fu Q, Wu T, Cui P, Fang G, Liu C, Chen C, Liu G, Wang W, Wang D, Wang P, Zhou D. Active iron phases regulate the abiotic transformation of organic carbon during redox fluctuation cycles of paddy soil. Environ Sci Technol, 2021, 55: 14281-14293

[3] Chen N, Huang D, Zeng Y, Wang J, Liu G, Liu X, Wu T, Gao Y, Fang G, Wang Y, Zhou D. Long-term application of agricultural amendments regulate hydroxyl radicals production during oxygenation of paddy soils. Environ Sci Technol, 2024, 58: 13509-13520

[4] Chen X, Song Y, Ling C, Shen Y, Zhan X, Xing B. Fate of emerging antibiotics in soil-plant systems: a case on fluoroquinolones. Sci Total Environ, 2024, 951: 75487

[5] Ginn B, Meile C, Wilmoth J, Tang Y, Thompson A. Rapid iron reduction rates are stimulated by high-amplitude redox fluctuations in a tropical forest soil. Environ Sci Technol, 2017, 51: 3250-3259

[6] Gligorovski S, Strekowski R, Barbati S, Vione D. Environmental implications of hydroxyl radicals (• OH). Chem Rev, 2015, 115: 13051-13092

[7] Huang D, Chen N, Zhu C, Sun H, Fang G, Zhou D. Dynamic production of hydroxyl radicals during the flooding–drainage process of paddy soil: an in situ column study. Environ Sci Technol, 2023, 57: 16340-16347

[8] Lee S-H, Hwang Y-M, Byun T-S, Ko J-H, Roh J-S. Effect of heating rate, temperature, and residence time during graphitization on the mechanical and electrical properties of isotropic graphite blocks. Carbon, 2023, 208: 443-451

[9] Li X, Tan M, Wu B, Wang J, Ma J, Chen B, Chu C. Redox oscillation-driven production of reactive oxygen species from black carbon. Environ Sci Technol, 2024, 58: 21210-21217

[10] Liu F, Ding Y, Liu J, Latif J, Qin J, Tian S, Sun S, Guan B, Zhu K, Jia H. The effect of redox fluctuation on carbon mineralization in riparian soil: an analysis of the hotspot zone of reactive oxygen species production. Water Res, 2024, 265 122294

[11] Luong DX, Bets KV, Algozeeb WA, Stanford MG, Kittrell C, Chen W, Salvatierra RV, Ren M, McHugh EA, Advincula PA. Gram-scale bottom-up flash graphene synthesis. Nature, 2020, 577: 647-651

[12] Page SE, Sander M, Arnold WA, McNeill K. Hydroxyl radical formation upon oxidation of reduced humic acids by oxygen in the dark. Environ Sci Technol, 2012, 46: 1590-1597

[13] Page SE, Kling GW, Sander M, Harrold KH, Logan JR, McNeill K, Cory RM. Dark formation of hydroxyl radical in arctic soil and surface waters. Environ Sci Technol, 2013, 47: 12860-12867

[14] Pan M, Chu LM. Adsorption and degradation of five selected antibiotics in agricultural soil. Sci Total Environ, 2016, 545: 48-56

[15] Qiu C, Jiang L, Gao Y, Sheng L. Effects of oxygen-containing functional groups on carbon materials in supercapacitors: a review. Mater des, 2023, 230 111952

[16] Shen L, Zhu X, Jiang H, Zhang J, Chen C, R. Reinfelder J, Kappler A, Fang L, Liu T, Liu C, Wu Y, Li F. Physical contact between bacteria and carbonaceous materials: the key switch triggering activated carbon and biochar to promote microbial iron reduction. Environ Sci Technol, 2025, 59: 9576-9586

[17] Strauss V, Marsh K, Kowal MD, El Kady M, Kaner RB. A simple route to porous graphene from carbon nanodots for supercapacitor applications. Adv Mater, 2018, 30 1704449

[18] Sun T, Levin BDA, Guzman JJL, Enders A, Muller DA, Angenent LT, Lehmann J. Rapid electron transfer by the carbon matrix in natural pyrogenic carbon. Nat Commun, 2017, 8 14873

[19] Sun T, Levin BDA, Schmidt MP, Guzman JJL, Enders A, Martínez CE, Muller DA, Angenent LT, Lehmann J. Simultaneous quantification of electron transfer by carbon matrices and functional groups in pyrogenic carbon. Environ Sci Technol, 2018, 52: 8538-8547

[20] Teng T, Wu X, Lu Y, Yu F, Jia C, Sun L, Lin L, He Z, Gao J, Zhang S. Flash reforming pyrogenic carbon to graphene for boosting advanced oxidation reaction. Adv Mater Technol, 2023, 8 2300236

[21] Tong M, Yuan S, Ma S, Jin M, Liu D, Cheng D, Liu X, Gan Y, Wang Y. Production of abundant hydroxyl radicals from oxygenation of subsurface sediments. Environ Sci Technol, 2016, 50: 214-221

[22] Wang B, Wolfe DE, Terrones M, Haque MA, Ganguly S, Roy AK. Electro-graphitization and exfoliation of graphene on carbon nanofibers. Carbon, 2017, 117: 201-207

[23] Wei L, Ge T, Zhu Z, Luo Y, Yang Y, Xiao M, Yan Z, Li Y, Wu J, Kuzyakov Y. Comparing carbon and nitrogen stocks in paddy and upland soils: accumulation, stabilization mechanisms, and environmental drivers. Geoderma, 2021, 398 115121

[24] Wu S, Fang G, Wang Y, Zheng Y, Wang C, Zhao F, Jaisi DP, Zhou D. Redox-active oxygen-containing functional groups in activated carbon facilitate microbial reduction of ferrihydrite. Environ Sci Technol, 2017, 51: 9709-9717

[25] Wu S, Wang D, Liu C, Fang G, Sun T-R, Cui P, Yan H, Wang Y, Zhou D. Pyridinic- and pyrrolic nitrogen in pyrogenic carbon improves electron shuttling during microbial Fe(III) reduction. ACS Earth Space Chem, 2021, 5: 900-909

[26] Wu NN, Liu S, Xu R, Huang QY, Pan YF, Li HX, Lin L, Hou R, Cheng YY, Xu XR. New insight into the bioaccumulation and trophic transfer of free and conjugated antibiotics in an estuarine food web based on multimedia fate and model simulation. J Hazard Mater, 2024, 465 133088

[27] Wu Y, Zhu Z, Sun P, Zhao Z, Zheng X, Long M, Chen Y. Enhanced short-chain fatty acids production from food waste with magnetic biochar via anaerobic fermentation: linking interfacial, extracellular, and intracellular electron transfer. Chem Eng J, 2024, 488 150853

[28] Xu H, Hei S, Fu W, Zhang X, Liang P, Pan B, Huang X. Unraveling the trade-off effect of pyrogenic carbons between biopseudocapacitors and bioconductors during anaerobic methanogenesis. Environ Sci Technol, 2025, 59: 2861-2874

[29] Yang Z, Sun T, Kleindienst S, Straub D, Kretzschmar R, Angenent LT, Kappler A. A coupled function of biochar as geobattery and geoconductor leads to stimulation of microbial Fe (III) reduction and methanogenesis in a paddy soil enrichment culture. Soil Biol Biochem, 2021, 163 108446

[30] Yang P, Wang S, Sun T, Jiang T, Cui Y, Liu G, Guo Y, Liu Y, Hu L, Shi J, Zhang Q, Yin Y, Cai Y, Jiang G. Fire-induced multiple changes in electron transfer properties of peat soil organic matter: the role of functional groups, graphitic carbon, and iron. Environ Sci Technol, 2024, 58: 20457-20467

[31] Yu W, Chu C, Chen B. Enhanced microbial ferrihydrite reduction by pyrogenic carbon: impact of graphitic structures. Environ Sci Technol, 2022, 56: 239-250

[32] Yu F, Jia C, Wu X, Sun L, Shi Z, Teng T, Lin L, He Z, Gao J, Zhang S. Rapid self-heating synthesis of Fe-based nanomaterial catalyst for advanced oxidation. Nat Commun, 2023, 14: 4975

[33] Yu W, Chu C, Chen B. Pyrogenic carbon improves Cd retention during microbial transformation of ferrihydrite under varying redox conditions. Environ Sci Technol, 2023, 57: 7875-7885

[34] Yuan S, Liu X, Liao W, Zhang P, Wang X, Tong M. Mechanisms of electron transfer from structrual Fe (II) in reduced nontronite to oxygen for production of hydroxyl radicals. Geochim Cosmochim Acta, 2018, 223: 422-436

[35] Zeng Q, Wang X, Liu X, Huang L, Hu J, Chu R, Tolic N, Dong H. Mutual interactions between reduced Fe-bearing clay minerals and humic acids under dark, oxygenated conditions: hydroxyl radical generation and humic acid transformation. Environ Sci Technol, 2020, 54: 15013-15023

[36] Zhang P, Yuan S, Liao P. Mechanisms of hydroxyl radical production from abiotic oxidation of pyrite under acidic conditions. Geochim Cosmochim Acta, 2016, 172: 444-457

[37] Zhang J, Xu X, Liang J, Huang W, Zhao L, Qiu H, Cao X. Natural attenuation of 2, 4-dichlorophenol in Fe-rich soil during redox oscillations: anoxic–oxic coupling mechanism. Environ Sci Technol, 2024, 58: 13467-13477

[38] Zhou GW, Yang XR, Sun AQ, Li H, Lassen SB, Zheng BX, Zhu YG. Mobile incubator for iron(III) reduction in the gut of the soil-feeding earthworm Pheretima guillelmi and interaction with denitrification. Environ Sci Technol, 2019, 53: 4215-4223

[39] Zhou G, Chen L, Zhang C, Ma D, Zhang J. Bacteria–virus interactions are more crucial in soil organic carbon storage than iron protection in biochar-amended paddy soils. Environ Sci Technol, 2023, 57: 19713-19722

[40] Zhu D, Wu H, Fong WK, Tabor RF, Zhang J. The ratio of sp² and sp³ hybridized carbon determines the performance of carbon‐based catalysts in H₂O₂ electrosynthesis from O₂. Angew Chem Int Ed, 2025, 64 e202500145

Funding

National Natural Science Foundation of China(22276040)

RIGHTS & PERMISSIONS

The Author(s)