Biochar-loaded AM fungi coupled with Arundo donax enable targeted red mud remediation via valency—specific metal detoxification and soil function recovery

Abstract

Abstract

Red mud, a saline-alkaline and metal-contaminated byproduct, poses severe ecological risks. This study elucidates the synergistic remediation mechanisms of biochar (BC) combined with arbuscular mycorrhizal fungi (AMF) in an Arundo donax-soil system. We specifically investigated biochar loaded with Funneliformis mosseae (BC–FM) and that loaded with Rhizophagus intraradices (BC–RI). The BC–FM treatment significantly enhanced the plant antioxidant system and photosynthetic capacity while reducing the content of exchangeable arsenic (As) and soil pH, thereby inducing a “photosynthesis enhancement-As immobilization” synergy. In contrast, the BC–RI treatment markedly increased plant biomass and soil microbial α–diversity, while simultaneously reducing the contents of soil lead (Pb) and sodium ions (Na⁺) and enhancing alkaline phosphatase activity—thus demonstrating a “Pb fixation–microbial diversity–soil phosphorus (P) activation” cascade. Rhizosphere network analysis identified key bacterial genera, with Longimicrobiaceae driving soil organic carbon accumulation in the BC–FM treatment and Lechevalieria enhancing alkaline phosphatase (ALP) activity in the BC–RI treatment. These findings support a novel “fungal species–heavy metal valency matching” principle, where RI preferentially targets cationic Pb, while FM targets anionic As. This principle establishes a three-dimensional synergistic model: “Heavy metal transformation–concurrent salinity-alkalinity mitigation–microbial function activation”. The results provide a foundational strategy for zonal red mud remediation: applying BC–RI in Pb–dominated areas and BC–FM in As–contaminated areas.

Highlights

•	Proposed “Fungal species−metal valency matching” enables zonal RM remediation: BC−RI for Pb, BC−FM for As.
•	The BC–FM synergy boosts photosynthesis and immobilizes As (V), thereby alleviating saline-alkali stress.
•	BC−RI enhances biomass, immobilizes Pb, diversifies the microbiota, and activates P.
•	Rhizosphere microbial networks reveal key genera (Longimicrobiaceae, Lechevalieria) driving C accumulation and ALP enhancement.

Keywords

Biochar-based inoculation / Co-contaminated soil / Salinity-alkalinity stress / Heavy metal toxicity / Arundo donax

References

[1] Alshaal T, Domokos-Szabolcsy É, Márton L, Czakó M, Kátai J, Balogh P, Elhawat N, El-Ramady H, Fári M. Phytoremediation of bauxite-derived red mud by giant reed. Environ Chem Lett, 2013, 11(3): 295-302

[2] Babzada SA, Raja V, Bhat AH, Qadir SU, Radhakrishnan A, Kumar N, Alsahli AA, Ahmad P. Alleviation of salinity stress by EDTA chelated-biochar and arbuscular mycorrhizal fungi on maize via modulation of antioxidants activity and biochemical attributes. J Hazard Mater, 2024, 24(1): 63

[3] Cappuyns V, Swennen R, Niclaes M. Application of the BCR sequential extraction scheme to dredged pond sediments contaminated by Pb−Zn mining: a combined geochemical and mineralogical approach. J Geochem Explor, 2007, 93278-90

[4] Chandra P, Singh A, Prajapat K, Rai AK, Yadav RK. Native arbuscular mycorrhizal fungi improve growth, biomass yield, and phosphorus nutrition of sorghum in saline and sodic soils of the semi-arid region. Environ Exp Bot, 2022, 201 104982

[5] Chen YL, Yang WT, Liu HY, Mao WJ, Zhang J, Wang B, Yang LY, Wang SS, Zhou H, Zeng P, Wu P. Phosphorus-loaded magnetic biochar for remediation of cadmium contaminated paddy soil: efficacy and identification of limiting factors. J Hazard Mater, 2025, 492 138162

[6] Chen RA, Chai XQ, Zhang YX, Zhou TX, Xia YY, Jiang XJ, Lv B, Zhang J, Zhou LX, Tian X, Wang RA, Mao LJ, Zhao F, Zhang HY, Hu J, Qiu JF, Zou Z, Chen CZ. Novel role of FTO in regulation of gut-brain communication via Desulfovibrio fairfieldensis−produced hydrogen sulfide under arsenic exposure. Gut Microbes, 2025, 17: 2438471

[7] Deng SG, Yang YF, Hu CY, Xiao SF, Kuzyakov Y, Liu CJ, Ma LQ. Arsenic uptake and metabolism in mycorrhizal As-hyperaccumulator Pteris vittata: symbiotic p transporters and as reductases. Environ Sci Technol, 2025, 59(11): 5556-5567

[8] Di Carlo E, Boullemant A, Courtney R. A field assessment of bauxite residue rehabilitation strategies. Sci Total Environ, 2019, 663: 915-926

[9] Di Carlo E, Boullemant A, Courtney R. Ecotoxicological risk assessment of revegetated bauxite residue: implications for future rehabilitation programmes. Sci Total Environ, 2019, 698 134344

[10] Dou ZW, Sun YH, Zhang YH, Wang MX, Zhang N, Liu AJ, Hu XX. Amelioration of the physicochemical properties enhanced the resilience of bacteria in bauxite residues. J Hazard Mater, 2024, 471 134455

[11] Essahibi A, Benhiba L, Fouad MO, Babram MA, Ghoulam C, Qaddoury A. Responsiveness of carob (Ceratonia siliqua L.) plants to arbuscular mycorrhizal symbiosis under different phosphate fertilization levels. J Plant Growth Regul, 2019, 38(4): 1243-1254

[12] Feng ZW, Liu XD, Qin YQ, Feng GD, Zhou Y, Zhu HH, Yao Q. Cooperation of arbuscular mycorrhizal fungi and bacteria to facilitate the host plant growth dependent on soil pH. Front Microbiol, 2023, 14: 1116943

[13] Gao JF. Experimental guidance for plant physiology, 2006, Beijing, Higher Education Press

[14] Garg N, Cheema A. Relative roles of arbuscular mycorrhizae in establishing a correlation between soil properties, carbohydrate utilization and yield in Cicer arietinum L. under As stress. Ecotoxicol Environ Saf, 2021, 207 111196

[15] Glinska S, Gapinska M. The effect of pre-incubation of Allium cepa L. roots in the ATH-rich extract on Pb uptake and localization. Protoplasma, 2013, 250(2): 601-611

[16] Gujre N, Agnihotri R, Rangan L, Sharma MP, Mitra S. Deciphering the dynamics of glomalin and heavy metals in soils contaminated with hazardous municipal solid wastes. J Hazard Mater, 2021, 416 125869

[17] Hao SY, Tian Y, Lin ZQ, Xie LZ, Zhou XB, Bañuelos GS. Effects of arbuscular mycorrhizal fungi on the reduction of arsenic accumulation in plants: a meta-analysis. Front Plant Sci, 2024, 15: 1327649

[18] He XX, Chen YQ, Liu SJ, Gunina A, Wang XL, Chen W, Shao YH, Shi LL, Yao Q, Li JX, Zou XM, Schimel JP, Zhang WX, Fu SL. Cooperation of earthworm and arbuscular mycorrhizae enhanced plant N uptake by balancing absorption and supply of ammonia. Soil Biol Biochem, 2018, 116: 351-359

[19] Hobbie EA, Jocher G, Peichl M, Zhao P, Zhou ZX, Hasselquist NJ. Ectomycorrhizal hydrophobicity and host association influence ectomycorrhizal C dynamics, N dynamics, and fruiting patterns in N addition experiments under pine. Plant Soil, 2025, 511(1–2): 867-883

[20] Lang M, Li X, Zheng CY, Li HG, Zhang JL. Shading mediates the response of mycorrhizal maize (Zea mays L.) seedlings under varying levels of phosphorus. Appl Soil Ecol, 2021, 166 104060

[21] Li TT, Yang H, Zhang NL, Dong LJ, Wu AP, Wu QQ, Zhao MS, Liu H, Li Y, Wang YH. Synergistic effects of arbuscular mycorrhizal fungi and biochar are highly beneficial to Ligustrum lucidum seedlings in Cd-contaminated soil. Environ Sci Pollut Res Int, 2023, 30(45): 11214-11227

[22] Li GH, Liu JJ, Yi LY, Luo J, Jiang T. Bauxite residue (red mud) treatment: current situation and promising solution. Sci Total Environ, 2024, 948 174757

[23] Li YL, Wu SJ, Jin ZX, Li JM. Differential strategies of two arbuscular mycorrhizal fungi varieties in the protection of Lycium ruthenicum under saline-alkaline stress. Plant Physiol Biochem, 2025, 222 109725

[24] Liu Y, Hu TS, Zhu R, Chen QW, Zeng X, Jing PR, Huang YF. A stomatal optimization model integrating leaf stomata−photosynthetic capacity regulation in response to soil water stress. Agric Water Manage, 2025, 308 109285

[25] Liu YW, Guan DX, Qiu LX, Luo Y, Liu F, Teng HH, Kuzyakov Y, Ma LQ. Spatial dynamics of phosphorus mobilization by mycorrhiza. Soil Biol Biochem, 2025, 206 109797

[26] Ma PK, Shi ZQ, Diao FW, Hao LJ, Zhang JX, Xu J, Wang LX, Dang ZH, Guo W. Effects of arbuscular mycorrhizal fungi on growth and Na plus accumulation of Suaeda glauca (Bunge) grown in salinized wetland soils. Appl Soil Ecol, 2021, 166 104065

[27] Nirukshan GS, Ranasinghe S, Sleutel S. The effect of biochar on mycorrhizal fungi mediated nutrient uptake by coconut (Cocos nucifera L.) seedlings grown on a Sandy Regosol. Biochar, 2023, 4 68

[28] Rijk I, Ekblad A, Dahlin AS, Enell A, Larsson M, Leroy P, Kleja DB, Tiberg C, Hallin S, Jones C. Biochar and peat amendments affect nitrogen retention, microbial capacity and nitrogen cycling microbial communities in a metal and polycyclic aromatic hydrocarbon contaminated urban soil. Sci Total Environ, 2024, 936 173454

[29] Robinson C, Schinner F, Ohlinger R, Kandeler E, Margesin R. Methods in soil biology. J Ecol, 1995, 85(3): 404

[30] Sarathambal C, Khankhane PJ, Gharde Y, Kumar B, Varun M, Arun S. The effect of plant growth—promoting rhizobacteria on the growth, physiology, and Cd uptake of Arundo donax L. Int J Phytoremediation, 2017, 194360-370

[31] Seshadri B, Bolan NS, Naidu R. Rhizosphere−induced heavy metal(loid) transformation in relation to bioavailability and remediation. J Plant Nutr Soil Sci, 2015, 178(2): 524-548

[32] Souza T, dos Santos JBL, Batista DS. Hydrogel and arbuscular mycorrhizal fungi inoculation as soil conditioners in dark Earth of the Amazon rainforest. J Soil Sediment, 2025, 25(5): 1487-1496

[33] Sun SK, Chen J, Zhao FJ. Regulatory mechanisms of sulfur metabolism affecting tolerance and accumulation of toxic trace metals and metalloids in plants. J Exp Bot, 2023, 74(11): 3286-3299

[34] Tóth C, Simon L, Tóth B. Microanatomical changes in the leaves of Arundo donax (l.) caused by potentially toxic elements from municipal sewage sediment. Plants, 2024, 13(5 740

[35] Videgain-Marco M, Marco-Montori P, Martí-Dalmau C, Jaizme-Vega MD, Manya-Cervello JJ, Garcia-Ramos FJ. The effects of biochar on indigenous arbuscular mycorrhizae fungi from agroenvironments. Plants-Basel, 2021, 105): 950

[36] Wang XH, Wang Y, Sun YQ, Wang KY, Yang JB, Zeng DJ, Mo L, Liao JX, Peng QS, Yao Y, Pu G. Soil polluted system shapes endophytic fungi communities associated with Arundo donax: a field experiment. PeerJ, 2025, 13 e18789

[37] Wen YQ, Wu RT, Xu TL, Cao RR, Song G, Qi DD, Chang W, Li K, Ping Y, Zhang MM, Fan XX, Song FQ. AMF and biochar reshape the bacterial network in rhizosphere soil of Ricinus communis under chromium (Cr) stress and improve soil quality. J Hazard Mater, 2025, 492 138122

[38] Xian KH, Su J, Fu CM, Huang NZ, Gong QF, He JX. Techniques for rapid propagation of Arundo donax. Guihaia, 2018, 381128-134

[39] Xie KH, Chen YX, Wang XQ, Zhou XY, Cheng YZ, Yu XC, Wang J, Sun MT, Li YS, He CX. Physiological and multi-omics analysis revealed the mechanism of arbuscular mycorrhizal fungi to cadmium toxicity in green onion. Ecotox Environ Safe, 2025, 290 117754

[40] Yang ZM, Zou ZD, Akhtar MA, Niu WJ, Ren LN, Zhang S, Liu N, Cao HL. Synergistic effects of N−containing heterocyclic and Ca ligand structures on the phosphorus adsorption of N/Ca co-doped biochar. J Clean Prod, 2021, 485 144392

[41] Yang JB, Wang XH, Wang KY, Zeng DJ, Mo L, Li S, Fang BZ, Rekadwad B, Li WJ, Pu GZ (2025) Mature Tiankengs are biodiversity hotspots of soil microorganisms in the karst region. Ecol Indic 170:113034

[42] Yuan XF, Deng YM, Gao J, Zheng TL, Xu YX, Wang YX. Unveiling the role of sulfate—reducing bacteria in arsenic methylation in alluvial-lacustrine aquifers. Water Res, 2025, 283 123864

[43] Zaman QU, Guo LH, He XR, Luo Y, Liu C, Murtaza G, Sultan K, Fahad S, Cheng X, Ashraf K, Deng G. Synergistic effect of arbuscular mycorrhizal fungi, biochar and seaweed extract for improving the copper tolerance in hemp. Ind Crop Prod, 2025, 224 120358

[44] Zhang D, Jiang QW, Liang DY, Huang SX, Liao JX. The potential application of giant reed (Arundo donax) in ecological remediation. Front Env Sci-Switz, 2021, 9 652367

[45] Zhang XL, Qiu YP, Gilliam FS, Gillespie CJ, Tu C, Reberg-Horton SC, Hu SJ. Arbuscular mycorrhizae shift community composition of N-cycling microbes and suppress soil N2O emission. Environ Sci Technol, 2022, 56(18): 13461-13472

[46] Zheng X, Li A, Nie RN, Wu CX, Ji XY, Tang JL, Zhang JP. Differential strategies of two arbuscular mycorrhizal fungi varieties in the protection of Lycium ruthenicum under saline-alkaline stress. J Fungi, 2024, 108554

[47] Zhou HY, Nian FZ, Chen BD, Zhu YG, Yue XR, Zhang NM, Xia YS. Synergistic reduction of arsenic uptake and alleviation of leaf arsenic toxicity in maize (Zea mays L.) by arbuscular mycorrhizal fungi (AMF) and exogenous iron through antioxidant activity. J Fungi, 2023, 96 677

[48] Zhu SX, Zhao W, Sun SX, Yang XQ, Mao H, Sheng LY, Chen ZB. Metagenomic analysis revealed N-metabolizing microbial response of Iris tectorum to Cr stress after colonization by arbuscular mycorrhizal fungi. Ecotoxicol Environ Saf, 2024, 273 116157

Funding

the National Natural Science Foundation of China(32460312)

the National Natural Science Foundation of Guangxi(2025GXNSFBA069005)

the Key Project of Natural Science Foundation of Heilongjiang Province(ZD2024C006)

the Fundamental Research Fund of the Guangxi Institute of Botany, China(Guizhiye)

the Key R&D Program of Guangxi, China(Guike AB22035038)

RIGHTS & PERMISSIONS

The Author(s)