Synergistic effects of Fe–Mn modified biochar and water management on remediation of Cd and Hg co-contaminated soils

Abstract

Cadmium (Cd) and mercury (Hg) contamination in paddy soils presents a formidable challenge to global food security and human health, primarily due to their contrasting biogeochemical behaviors under varying water management regimes. This study investigated an integrated remediation strategy combining iron–manganese oxide modified biochar (FMBC) application with two distinct water management regimes (continuous flooding and aerobic irrigation) to synergistically mitigate Cd and Hg accumulation in rice and elucidate their underlying mechanisms, including the impacts on soil microbial communities. Pot experiments revealed that continuous flooding effectively decreased soil Cd bioavailability and promoted iron−manganese oxide plaque (IMP) formation on the root surface, thereby impeding Cd uptake. Conversely, this condition inadvertently promoted the relative abundance of hgcA-containing methylating microorganisms, thereby elevating the risk of Hg methylation. In contrast, aerobic irrigation reduced total Hg (THg) and methylmercury (MeHg) accumulation in rice grains, yet concurrently exacerbated Cd uptake by the plants. The incorporation of FMBC effectively resolved this antagonistic dilemma through dual immobilization mechanisms. Specifically, the combination of continuous flooding and FMBC application minimized grain Cd concentration (0.05 mg kg⁻¹), while simultaneously suppressing the flooding-induced proliferation of hgcA-containing microbes. Conversely, integrating aerobic irrigation with FMBC achieved the lowest grain THg (0.02 mg kg⁻¹) and MeHg (6.89 μg kg⁻¹) levels, while simultaneously restricting aerobic-induced Cd uptake. Overall, the synergistic integration of FMBC with specific water management provides a highly effective and sustainable strategy for mitigating both Cd and Hg bioaccumulation in rice grains, thereby enhancing food safety in co-contaminated paddy ecosystems.

Graphical Abstract

Keywords

Cd–Hg co-contamination / Fe–Mn modified biochar / Water management / Bacterial community / Oryza sativa L.

References

[1] Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, Thomas BC, Singh A, Wilkins MJ, Karaoz U, Brodie EL, Williams KH, Hubbard SS, Banfield JF. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun, 2016, 7: 13219.

[2] Bao SD. Analysis methods of soil agricultural chemistry, 2000. Beijing, China Agricultural Science and Technology Publishing House

[3] Bao Q, Shi J, Liu Z, Kan Y, Bao W. Application of crop straw with different C/N ratio affects CH4 emission and Cd accumulation in rice (Oryzasativa L.) in Cd polluted paddy soils. Clim Smart Agr, 2025, 2: 100036.

[4] Bi W, Weng B, Yan D, Wang M, Wang H, Wang J, Yan H. Effects of drought–flood abrupt alternation on phosphorus in summer maize farmland systems. Geoderma, 2020, 363: 114147.

[5] Cang L, Xing J, Liu C, Wang Y, Zhou D. Effects of different water management strategies on the stability of cadmium and copper immobilization by biochar in rice–wheat rotation system. Ecotoxicol Environ Saf, 2020, 202: 110887.

[6] Carrijo DR, Lundy ME, Linquist BA. Rice yields and water use under alternate wetting and drying irrigation: a meta–analysis. Field Crops Res, 2017, 203: 173-180.

[7] Chang C, Chen C, Yin R, Shen Y, Mao K, Yang Z, Feng X, Zhang H. Bioaccumulation of Hg in rice leaf facilitates selenium bioaccumulation in rice (Oryza sativa L.) leaf in the Wanshan mercury mine. Environ Sci Technol, 2020, 54: 3228-3236.

[8] Cheng H, Wang M, Wong MH, Ye Z. Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues?. Plant Soil, 2014, 375: 137-148.

[9] Delaune RD, Jugsujinda A, Devai I, Patrick WH. Relationship of sediment redox conditions to methyl mercury in surface sediment of Louisiana Lakes. J Environ Sci Health A Tox Hazard Subst Environ Eng, 2004, 39: 1925-1933.

[10] Fabbrini M, Scicchitano D, Candela M, Turroni S, Rampelli S. Connect the dots: sketching out microbiome interactions through networking approaches. Microbiome Res Rep, 2023, 2: 25.

[11] Furuya M, Hashimoto Y, Yamaguchi N. Time–course changes in speciation and solubility of cadmium in reduced and oxidized paddy soils. Soil Sci Soc Am J, 2016, 80: 870-877.

[12] Grigg BC, Beyrouty CA, Norman RJ, Gbur EE, Hanson MG, Wells BR. Rice responses to changes in floodwater and N timing in southern USA. Field Crops Res, 2000, 66: 73-79.

[13] Guo M, Gao J, Yang M, Liu Y, Fu J, Ma R, Xiong F, Zhang T, Liu X, Jin Y, Qu J. Synergistic effects of PGPR and organic fertilizer on soil fertility, enzyme activities, and microbial community composition in saline–alkali rice systems. Appl Soil Ecol, 2025, 213: 106327.

[14] He Y, Yang X, Li Z, Wang T, Ma C, Wen X, Chen W, Zhang C. Aging rice straw reduces the bioavailability of mercury and methylmercury in paddy soil. Chemosphere, 2023, 339: 139711.

[15] Hu P, Ouyang Y, Wu L, Shen L, Luo Y, Christie P. Effects of water management on arsenic and cadmium speciation and accumulation in an upland rice cultivar. J Environ Sci, 2015, 27: 225-231.

[16] Huang G, Ding X, Liu Y, Zeng L, Chen R, Wang S, Tang Z, Zhou Y, Wang J. Liming and tillering application of manganese alleviates iron manganese plaque reduction and cadmium accumulation in rice (Oryzasativa L.). J Hazard Mater, 2022, 427: 127897.

[17] Huang Y, Yi J, Huang Y, Zhao S, Zhou B, Wang J, Zhu Y, Du Y, Li F. Insights into the reduction of methylmercury accumulation in rice grains through biochar application: Hg transformation, isotope fractionation, and transcriptomic analysis. Environ Pollut, 2024, 340: 122863.

[18] Jiang M, Li C, Gao W, Cai K, Tang Y, Cheng J. Comparison of long–term effects of biochar application on soil organic carbon and its fractions in two ecological sites in karst regions. Geoderma Reg, 2022, 28: e00477.

[19] Jin M, Xiao A, Zhu L, Zhuang Z, Zhao G, Jiang L. The diversity and commonalities of the radiation–resistance mechanisms of Deinococcus and its up–to–date applications. AMB Express, 2019, 9: 138.

[20] Kong Z, Wu Z, Glick BR, He S, Huang C, Wu L. Co–occurrence patterns of microbial communities affected by inoculants of plant growth–promoting bacteria during phytoremediation of heavy metal–contaminated soils. Ecotoxicol Environ Saf, 2019, 183: 109504.

[21] Kong F, Guan DX, Huang P, Lu S, Xu J, Wang H. Unveiling the barriers of Cd translocation from soil to rice: insights from continuous flooding. Sci Total Environ, 2024, 946: 174265.

[22] Li J, Xu Y. Immobilization remediation of Cd–polluted soil with different water condition. J Environ Manage, 2017, 193: 607-612.

[23] Li T, Zhou H, Zhang J, Zhang Z, Yu Y, Wei Y, Hu J. Effects of silkworm excrement and water management on the accumulation of Cd and As in different varieties of rice and an assessment of their health risk. Ecotoxicol Environ Saf, 2021, 228: 112974.

[24] Li X, Li X, Li Y, et al.. Improved immobilization of soil cadmium by regulating soil characteristics and microbial community through reductive soil disinfestation. Sci Total Environ, 2021.

[25] Li H, Zhang H, Yang Y, Fu G, Tao L, Xiong J. Effects and oxygen–regulated mechanisms of water management on cadmium (Cd) accumulation in rice (Oryza sativa). Sci Total Environ, 2022, 846: 157484.

[26] Li X, Zhou J, Zhou T, Li Z, Hu P, Luo Y, Christie P, Wu L. Potential mobilization of cadmium and zinc in soils spiked with smithsonite and sphalerite under different water management regimes. J Environ Manage, 2022, 324: 116336.

[27] Li Y, Lu C, Zhu N, Chao J, Hu W, Zhang Z, Wang Y, Liang L, Chen J, Xue D, Gao Y, Zhao J. Mobilization and methylation of mercury with sulfur addition in paddy soil: implications for integrated water–sulfur management in controlling Hg accumulation in rice. J Environ Manage, 2022, 430: 128447.

[28] Li Y, Wei S, Chen X, Dong Y, Zeng M, Yan C, Hou L, Jiao R. Isolation of cadmium–resistance and siderophore–producing endophytic bacteria and their potential use for soil cadmium remediation. Heliyon, 2023, 9: e17661.

[29] Li J, Gao Y, Li C, Wang F, Chen H, Yang X, Jeyakumar P, Sarkar B, Luo Z, Bolan N, Li X, Meng J, Wang H. Pristine and Fe–functionalized biochar for the simultaneous immobilization of arsenic and antimony in a contaminated mining soil. J Hazard Mater, 2024, 469: 133937.

[30] Liang T, Chang D, Zhou G, Cai C, Liu R, Sun J, Gao S, Ma Z, Xie J, Shi S, Nie J, Liao Y, Cao W. A comprehensive strategy for solving Cd risk while improving soil quality and rice yield in paddy fields: co–utilizing green manure, rice straw, and biochar. J Hazard Mater, 2025, 500: 140372.

[31] Lindsay WL, Norvell WA. Development of a DTPA soil test for Zinc, Iron, Manganese, and Copper. Soil Sci Soc Am J, 1978, 42: 421-428.

[32] Liu Z, Wang Q, Huang S, Kong L, Zhuang Z, Wang Q, Li H, Wan Y. The risks of sulfur addition on cadmium accumulation in paddy rice under different water–management conditions. J Environ Sci, 2022, 118: 101-111.

[33] Liu C, Ning Y, Liu J. Geochemical mercury pools regulate diverse communities of hgcA microbes and MeHg levels in paddy soils. Environ Pollut, 2023, 334: 122172.

[34] Liu X, Guo J, Xue L, Zhao D, Liu G. Where has all the rice gone in China? A farm–to–fork material flow analysis of rice supply chain with uncertainty analysis. Resour Conserv Recycl, 2023, 190: 106853.

[35] Liu Y, Ma J, Chu J, Sun W, Wang Q, Liu Y, Zou P, Ma J. Machine learning and structural equation modeling for revealing the influence factors and pathways of different water management regimes acting on brown rice cadmium. Sci Total Environ, 2024, 954: 176033.

[36] Lu RK. Methods of soil and agro–chemical analysis, 2000. Beijing, China Agricultural Science and Technology Press

[37] Luo S, Liu Y, Luo B, Yang Y, Li L, Fu X, Peng L, Zeng Q. Straw removal or non–removal affects cadmium (Cd) accumulation in soil–rice (Oryzasativa L.) system at different ambient air Cd levels. J Environ Manage, 2023, 344: 118477.

[38] Luo W, Yang S, Khan M, Ma J, Xu W, Li Y, Xiang Z, Jin G, Jia J, Zhong B, Duan L, Zhu Y, Liu D. Mitigation of Cd accumulation in rice with water management and calcium–magnesium phosphate fertilizer in field environment. Geochem Health, 2020, 42: 3877-3886.

[39] Mai X, Tang J, Tang J, Zhu X, Yang Z, Liu X, Zhuang X, Feng G, Tang L. Research progress on the environmental risk assessment and remediation technologies of heavy metal pollution in agricultural soil. J Environ Sci, 2025, 149: 1-20.

[40] Man Y, Wang B, Wang J, Slaný M, Yan H, Li P, El-Naggar A, Shaheen SM, Rinklebe J, Feng X. Use of biochar to reduce mercury accumulation in Oryza sativa L: a trial for sustainable management of historically polluted farmlands. Environ Int, 2021, 153: 106527.

[41] MEP, MLR (Ministry of Environmental Protection, Ministry of Land and Resources, PRC). The national soil pollution status survey bulletin, 2014. Beijing, China Environmental Science Press

[42] Nie T, Liu H, Chen P, Li Y, Wang Y, Zhang H. Straw return combined with water–saving irrigation improves soil quality and rice yield by regulating microbial community structure in paddy fields. Appl Soil Ecol, 2025, 214: 106402.

[43] Pan Y, Koopmans GF, Bonten LTC, Song J, Luo Y, Temminghoff EJM, Comans RNJ. Temporal variability in trace metal solubility in a paddy soil not reflected in uptake by rice (Oryza sativa L.). Environ Geochem Health, 2016, 38: 1355-1372.

[44] Peng X, Liu F, Wang W, Ye Z. Reducing total Mercury and methylmercury accumulation in rice grains through water management and deliberate selection of rice cultivars. Environ Pollut, 2012, 162: 202-208.

[45] Huang Q, Liu Y, Qin X, Zhao L, Liang X, Xu Y. Selenite mitigates cadmium–induced oxidative stress and affects Cd uptake in rice seedlings under different water management systems. Ecotox Environ Safe, 2019, 168: 486-494.

[46] Ran S, He T, Zhou X, Yin D. Effects of fulvic acid and humic acid from different sources on Hg methylation in soil and accumulation in rice. J Environ Sci, 2022, 119: 93-105.

[47] Ran S, Li H, Yu Y, Zhu T, Dao J, Long S, Cai J, Liu TY, Xu Y. Ecological characteristics of tall fescue and spatially organized communities: their contribution to mitigating Cadmium damage. J Hazard Mater, 2024, 480: 135953.

[48] Rothenberg SE, Anders M, Ajami NJ, Petrosino JF, Balogh E. Water management impacts rice methylmercury and the soil microbiome. Sci Total Environ, 2016, 572: 608-617.

[49] Sun T, Sun Y, Xu Y, Wang L, Liang X. Effective removal of Hg²⁺ and Cd²⁺ in aqueous systems by Fe–Mn oxide modified biochar: a combined experimental and DFT calculation. Desalination, 2023, 549: 116306.

[50] Sun T, Gao G, Yang W, Sun Y, Huang Q, Wang L, Liang X. High–efficiency remediation of Cd and Hg co–contaminated paddy soils by Fe–Mn oxide modified biochar and its microbial community responses. Biochar, 2024, 6: 56.

[51] Tang S, Zhou H, Tan W, Huang J, Zeng P, Gu J, Liao B. Adsorption characteristics and mechanisms of Fe–Mn oxide modified biochar for Pb(II) in wastewater. Int J Environ Res Public Health, 2022, 19: 8420.

[52] Taylor G, Crowde A. Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot, 1983, 70: 1254-1257.

[53] Tessier A, Campbell PGC, Bisson M. Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem, 1979, 51: 844-851.

[54] Tian T, Zhou H, Gu J, Jia R, Li H, Wang Q, Zeng M, Liao B. Cadmium accumulation and bioavailability in paddy soil under different water regimes for different growth stages of rice (Oryza sativa L.). Plant Soil, 2019, 440: 327-339.

[55] Tian L, Guan W, Ji Y, He X, Chen W, Alvarez PJJ, Zhang T. Microbial methylation potential of mercury sulfide particles dictated by surface structure. Nat Geosci, 2021, 14: 409-416.

[56] Tian T, Yu L, Feng R, Yao C, Gong L, Xiao H, Liu L, Li F. Unveiling the combined effects of water management and lime on remediation of Cd–contaminated soils with improved soil quality. J Environ Chem Eng, 2024, 12: 114778.

[57] Wan Y, Liu J, Zhuang Z, Wang Q, Li H. Heavy metals in agricultural soils: sources, influencing factors, and remediation strategies. Toxics, 2024, 12: 63.

[58] Wang X, Ye Z, Li B, Huang L, Meng M, Shi J, Jiang G. Growing rice aerobically markedly decreases mercury accumulation by reducing both Hg bioavailability and the production of MeHg. Environ Sci Technol, 2014, 48: 1878-1885.

[59] Wang M, Chen S, Chen L, Wang D, Zhao C. The responses of a soil bacterial community under saline stress are associated with Cd availability in long–term wastewater–irrigated field soil. Chemosphere, 2019, 236: 124372.

[60] Wang M, Tang Z, Chen X, Wang X, Zhou W, Tang Z, Zhang J, Zhao F. Water management impacts the soil microbial communities and total arsenic and methylated arsenicals in rice grains. Environ Pollut, 2019, 247: 736-744.

[61] Wang Y, Dang F, Zheng X, Zhong H. Biochar amendment to further reduce methylmercury accumulation in rice grown in selenium–amended paddy soil. J Hazard Mater, 2019, 365: 590-596.

[62] Wang Y, Sun Y, He T, Deng H, Wang Z, Wang J, Zheng X, Zhou L, Zhong H. Biochar amendment mitigates the health risks of dietary methylmercury exposure from rice consumption in mercury–contaminated areas. Environ Pollut, 2020, 267: 115547.

[63] Wang M, Wang L, Zhao S, Li S, Lei X, Qin L, Sun X, Chen S. Manganese facilitates cadmium stabilization through physicochemical dynamics and amino acid accumulation in rice rhizosphere under flood–associated low pe+pH. J Hazard Mater, 2021, 416: 126079.

[64] Wang X, Lu X, Li Z, Cheng Q, Zhou Y, Lei M. Liming alters microbial community composition and its co–occurrence patterns in Cd– and Pb–contaminated agricultural soil. Appl Soil Ecol, 2021, 166: 103996.

[65] Wang YL, Ikuma K, Brown AMV, DeLevie A. Global survey of hgcA–carrying genomes in marine and freshwater sediments: insights into mercury methylation processes. Environ Pollut, 2024, 352: 124117.

[66] Wu XH, Wang W, Yin CM, Hou HJ, Xie KJ, Xie XL. Water consumption, grain yield, and water productivity in response to field water management in double rice systems in China. PLoS ONE, 2017, 12: e0189280.

[67] Wu Y, Jiang Z, Ma L, Wu X, Lu Q, Zang S. Enhanced stability of bacterial co–occurrence networks to biochar amendment reduces soil carbon mineralization in permafrost–affected soils. Int Biodeterior Biodegrad, 2026, 207: 106224.

[68] Xia W, Ghouri F, Zhong M, Bukhari SAH, Ali S, Shahid MQ. Rice and heavy metals: a review of cadmium impact and potential remediation techniques. Sci Total Environ, 2024, 957: 177403.

[69] Xiao W, Ye X, Zhu Z, Zhang Q, Zhao S, Chen D, Gao N, Hu J. Continuous flooding stimulates root iron plaque formation and reduces chromium accumulation in rice (Oryzasativa L.). Sci Total Environ, 2021, 788: 147786.

[70] Xiao W, Ye X, Ye Z, Zhang Q, Zhao S, Chen D, Gao N, Huang M. Responses of microbial community composition and function to biochar and irrigation management and the linkage to Cr transformation in paddy soil. Environ Pollut, 2022, 304: 119232.

[71] Xing Y, Wang J, Kinder CES, Yang X, Slaný M, Wang B, Song H, Shaheen SM, Leinweber P, Rinklebe J. Rice hull biochar enhances the mobilization and methylation of mercury in a soil under changing redox conditions: implication for Hg risks management in paddy fields. Environ Int, 2022, 168: 107484.

[72] Xu J, Peng S, Qiao Z, Yang S, Gao X. Binding forms and availability of Cd and Cr in paddy soil under non–flooding controlled irrigation. Paddy Water Environ, 2014, 12: 213-222.

[73] Xu X, Han J, Pang J, Wang X, Lin Y, Wang Y, Qiu G. Methylmercury and inorganic mercury in Chinese commercial rice: Implications for overestimated human exposure and health risk. Environ Pollut, 2020, 258: 113706.

[74] Xu W, Hou S, AmanKhan M, Yu C, Xiao L, Ruan Z, Liu H, Chen Z, Ceng S, Ye Z, Liu D. Effect of water and fertilization management on Cd immobilization and bioavailability in Cd–polluted paddy soil. Chemosphere, 2021, 276: 130168.

[75] Yan B, Liu N, Liu M, Du X, Shang F, Huang Y. Soil actinobacteria tend to have neutral interactions with other co-occurring microorganisms, especially under oligotrophic conditions. Environ Microbiol, 2021, 23: 4126-4140.

[76] Yan K, You Q, Wang S, Zou Y, Chen J, Xu J, Wang H. Depth–dependent patterns of soil microbial community in the E–waste dismantling area. J Hazard Mater, 2023, 444: 130379.

[77] Yang W, Sun T, Sun Y. Adsorption mechanism of Cd²⁺ on microbial inoculant and its potential for remediation Cd–polluted farmland soils. Chemosphere, 2024, 352: 141349.

[78] Yao Q, Liu J, Yu Z, Li Y, Jin J, Liu X, Wang G. Changes of bacterial community compositions after three years of biochar application in a black soil of northeast China. Appl Soil Ecol, 2017, 113: 11-21.

[79] Yao B, Wang S, Xie S, Li G, Sun G. Optimal soil Eh, pH for simultaneous decrease of bioavailable Cd, As in co–contaminated paddy soil under water management strategies. Sci Total Environ, 2022, 806: 151342.

[80] Yin D, Wang X, Peng B, Tan C, Ma LQ. Effect of biochar and Fe–biochar on Cd and As mobility and transfer in soil–rice system. Chemosphere, 2017, 186: 928-937.

[81] Zeng P, Wei B, Zhou H, Gu J, Liao B. Co–application of water management and foliar spraying silicon to reduce cadmium and arsenic uptake in rice: a two–year field experiment. Sci Total Environ, 2022, 818: 151801.

[82] Zhang Q, Chen H, Huang D, Xu C, Zhu H, Zhu Q. Water managements limit heavy metal accumulation in rice: dual effects of iron–plaque formation and microbial communities. Sci Total Environ, 2019, 687: 790-799.

[83] Zhang H, Ruan C, Chen L, Fan X, Jia F, Tong J, Zhang C, Shi J. Microbial mechanical insights into the cadmium accumulation of rice (Oryzasativa L.) grains in Cd–contaminated seleniferous paddy soils: a data–driven observational research. J Hazard Mater, 2025, 494: 138426.

[84] Zhao F, Wang P. Arsenic and cadmium accumulation in rice and mitigation strategies. Plant Soil, 2020, 446: 1-21.

[85] Zhao L, Meng B, Feng X. Mercury methylation in rice paddy and accumulation in rice plant: a review. Ecotoxicol Environ Saf, 2020, 195: 110462.

[86] Zhao F, Wang J, Li Y, Xu X, He L, Wang J, Ren C, Guo Y. Microbial functional genes driving the positive priming effect in forest soils along an elevation gradient. Soil Biol Biochem, 2022, 165: 108498.

[87] Zhao L, Song J, Hu H, White JJ, Ji X, Gond SK, Wang B, Li H. Mercury–driven fungal endophytic community and the role of endophytes in rice grain mercury accumulation. Curr Res Microb Sci, 2026, 10: 100525.

[88] Zhou Q, Liao B, Lin L, Qiu W, Song Z. Adsorption of Cu(II) and Cd(II) from aqueous solutions by ferromanganese binary oxide–biochar composites. Sci Total Environ, 2018, 615: 115-122.

[89] Zhu Q, Huang D, Liu S, Zhou B, Luo Z, Zhu H. Flooding–enhanced immobilization effect of sepiolite on cadmium in paddy soil. J Soils Sediments, 2012, 12: 169-177.

Funding

Natural Science Foundation of Tianjin(25JCZDJC00370)

Innovation Program of Chinese Academy of Agricultural Sciences(CAAS–SCAGLC–202301)

Central Public-interest Scientific Institution Basal Research Fund, Chinese Academy of Fishery Sciences(Y2025YC128)

China Postdoctoral Science Foundation Postdoctoral Fellowship Program(GZC20241904)

China Postdoctoral Science Foundation Funded Project(2024M763519)

RIGHTS & PERMISSIONS

The Author(s)