Synergistic enhancement of soil multifunctionality by biochar and arbuscular mycorrhizal fungi via improved nutrient supply in coal mining reclaimed soils

Abstract

Coal mining activities cause the destruction of surface vegetation, degradation of the soil structure, and severe loss of organic matter, thereby reducing soil multifunctionality. Biochar (BIO) and arbuscular mycorrhizal fungi (AMF) play crucial roles in mediating soil quality and crop production, especially in resource-constrained poor soils. However, little research has documented the synergistic effects of BIO + AMF on soil multifunctionality in coal-mine reclamation areas. Here, a three-year field investigation was carried out to evaluate the effects of four treatments: CK (traditional planting, no AMF and no BIO), AMF (AMF without biochar), BIO (biochar without AMF), and BIO + AMF (biochar and AMF). The findings demonstrated that the BIO + AMF treatment significantly modified the soil physical structure, increasing the soil water retention while decreasing the soil bulk density. The application of biochar supplemented with AMF notably increased the soil enzyme activity, nutrient supply, and the alpha and beta diversities of the soil bacterial and fungal communities. Moreover, biochar and AMF synergistically enhanced soil multifunctionality, and a random forest model revealed that the combination of AMF inoculation and biochar application increased maize production, which was driven mainly by soil enzyme activity, and that soil multifunctionality was regulated mainly by the nutrient supply function. These results highlight that biochar combined with AMF inoculation had significant synergistic effects on improving maize productivity and multifunctionality, providing a nature-based restoration strategy for use in reclaimed soil.

Graphical Abstract

Keywords

Biochar / Arbuscular mycorrhizal fungi / Synergistic effect / Soil multifunctionality / Coal mining reclaimed soil

Highlight

•	AMF and biochar regulated reclaimed soil function via improved structure, microbial diversity, and nutrient cycling.
•	AMF + biochar synergistically increased soil nutrient supply to boost reclaimed soil multifunctionality.
•	This research presents a nature-based strategy for restoring degraded land and realizing the potential for sustainability in reclaimed soils.

References

[1] Abbott LK, MacDonald LM, Wong MTF, Webb MJ, Jenkins SN, Farrell M. Potential roles of biological amendments for profitable grain production - a review. Agric Ecosyst Environ, 2018, 256: 34-50.

[2] Abdalla M, Bitterlich M, Jansa J, Pueschel D, Ahmed MA. The role of arbuscular mycorrhizal symbiosis in improving plant water status under drought. J Exp Bot, 2023, 74(16): 4808-4824.

[3] Allen AP, Gillooly JF. Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett, 2009, 12(5): 369-384.

[4] Amoakwah E, Arthur E, Frimpong KA, Lorenz N, Rahman MA, Nziguheba G, Islam KF. Biochar amendment impacts on microbial community structures and biological and enzyme activities in a weathered tropical sandy loam. Appl Soil Ecol, 2022, 172. ArticleID: 104364

[5] Bao SD. Soil and agricultural chemistry analysis, 2000China Agriculture Press

[6] Bo H, Li Z, Wang W, Zhang R, Wang H, Jin D, Xu M, Zhang Q. Combining organic and inorganic fertilization enhances soil enzyme activity, the bacterial community, and molecular ecological network complexity in coal mine reclamation areas. Agronomy, 2024, 14. ArticleID: 1427

[7] Camenzind T, Mason-Jones K, Mansour I, Rillig MC, Lehmann J. Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nat Geosci, 2023, 16: 115-122.

[8] Cen R, Feng W, Yang F, Wu W, Liao H, Qu Z. Effect mechanism of biochar application on soil structure and organic matter in semi-arid areas. J Environ Manage, 2021, 286. ArticleID: 112198

[9] Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, Pan G, Li L, Zheng J, Zhang X, Wang J. Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China. Appl Soil Ecol, 2013, 71: 33-44.

[10] Chen Y, Yu X, Xu D, Peng J. A spatial machine learning approach to exploring the impacts of coal mining and ecological restoration on regional ecosystem health. Environ Res, 2025, 264(2. ArticleID: 120379

[11] Chen ZM, Xiao X, Chen BL, Zhu LZ. Quantification of chemical states, dissociation constants and contents of oxygen-containing groups on the surface of biochars produced at different temperatures. Environ Sci Technol, 2015, 49(1): 309-317.

[12] Cheng H, Wang J, Tu C, Lin S, Xing D, Hill P, Chadwick D, Jones LD. Arbuscular mycorrhizal fungi and biochar influence simazine decomposition and leaching. GCB Bioenergy, 2020, 13: 708-718.

[13] Dai M, Hamel C, Bainard LD, Arnaud MS, Grant CA, Lupwayi NZ, Malhi SS, Lemke R. Negative and positive contributions of arbuscular mycorrhizal fungal taxa to wheat production and nutrient uptake efficiency in organic and conventional systems in the Canadian prairie. Soil Biol Biochem, 2014, 74: 156-166.

[14] Das P, Barker C, Park Y, Perreault F, Westerhoff P, Penton CR. Impact of graphite nano amendments on soil enzyme activities, functional genes and microbiome composition in a soil-plant system. Soil Biol Biochem, 2025, 203. ArticleID: 109714

[15] Degens BP. Macro-aggregation of soils by biological bonding and binding mechanisms and the factors affecting these: a review. Soil Res, 1997, 35(3): 431-460.

[16] Della MIF, Godeas AM, Scervino JM. In vivo modulation of arbuscular mycorrhizal symbiosis and soil quality by fungal P solubilizers. Microb Ecol, 2020, 79(1): 21-29.

[17] Duan HX, Luo CL, Li JY, Wang BZ, Naseer M, Xiong YC. Improvement of wheat productivity and soil quality by arbuscular mycorrhizal fungi is density- and moisture-dependent. Agron Sustain Dev, 2021, 41. ArticleID: 3

[18] Duarte SD, Cerri CEP, Rittl TF, Abbruzzin TF, Pano BLP. Biochar physical and hydrological characterization to improve soil attributes for plant production. J Soil Sci Plant Nutr, 2023, 23(3): 3051-3057.

[19] Gill J, Tharp CL, Suseela V. Arbuscular mycorrhizal symbiosis enables efficient phosphorus uptake in sorghum accessions with contrasting root traits. Plant Cell Environ, 2025.

[20] Goswami S. Impact of coal mining on environment. Eur Res, 2015, 92(3): 185-196.

[21] Gu W, Wang Y, Feng Z, Wu D, Zhang H, Yuan H, Sun Y, Xiu L, Chen W, Zhang W. Long-term effects of biochar application with reduced chemical fertilizer on paddy soil properties and japonica rice production system. Front Environ Sci, 2022, 10. ArticleID: 902752

[22] Gujre N, Soni A, Rangan L, Tsang DCW, Mitra S. Sustainable improvement of soil health utilizing biochar and arbuscular mycorrhizal fungi: a review. Environ Pollut, 2021, 268. ArticleID: 115549

[23] Guo J, Zhou H, Jia L, Wang Y, Fan M. Effects of biochar from different pyrolysis temperatures on soil physical properties and hydraulic characteristics in potato farmland of arid and semi-arid regions. Agric Water Manag, 2025, 313. ArticleID: 109483

[24] Hammer EC, Balogh-Brunstad Z, Jakobsen I, Olsson PA, Stipp SLS, Rillig MC. A mycorrhizal fungus grows on biochar and captures phosphorus from its surfaces. Soil Biol Biochem, 2014, 77: 252e-260.

[25] Han LF, Zhang B, Chen LY, Feng YF, Yang Y, Sun K. Impact of biochar amendment on soil aggregation varied with incubation duration and biochar pyrolysis temperature. Biochar, 2021, 3(3): 339-347.

[26] Han S, Liang Y, Zhang DS, Wang Y. Effects of combined application of biochar and arbuscular mycorrhizal fungi on soil organic carbon content and stability. J Agro-Environ Sci, 2026, 45(1): 127-138.

[27] Hu W, Ran J, Dong L, Du Q, Ji M, Yao S, Sun Y, Gong C, Hou Q, Gong H, Chen R, Lu J, Xie S, Wang Z, Huang H, Li X, Xiong J, Xia R, Wei M, Zhao D, Zhang Y, Li J, Yang H, Wang X, Deng Y, Sun Y, Li H, Zhang L, Chu Q, Li X, Aqeel M, Manan A, Akram MA, Liu X, Li R, Li F, Hou C, Liu J, He J, An L, Bardgett RD, Schmid B, Deng J. Aridity-driven shift in biodiversity-soil multifunctionality relationships. Nat Commun, 2021, 12. ArticleID: 5350

[28] Hu W, Zhang Y, Rong X, Zhou X, Fei J, Peng J, Luo G. Biochar and organic fertilizer applications enhance soil functional microbial abundance and agroecosystem multifunctionality. Biochar, 2024, 6: 3.

[29] Jia A, Song X, Li S, Liu Z, Liu X, Han Z, Gao H, Gao Q, Zha Y, Liu Y, Wu X. Biochar enhances soil hydrological function by improving the pore structure of saline soil. Agric Water Manag, 2024, 306. ArticleID: 109170

[30] Jing X, Sanders NJ, Shi Y, Chu H, Classen AT, Zhao K, Chen L, Shi Y, Jiang Y, He JS. The links between ecosystem multifunctionality and above-and belowground biodiversity are mediated by climate. Nat Commun, 2015, 6: 1-8.

[31] Li MY, Hu HB, Jin W, Ge ZW, Sun HJ, Tang ZL, Liu X. Effects of biochar combined with salt-tolerant trees on phosphorus cycling bacterial community in intertidal saline soil. Acta Ecol Sin, 2026, 46(10): 1-14.

[32] Li SQ, Chi SQ, Lin CQ, Cai C, Yang LH, Peng KM, Huang XF, Liu J. Combination of biochar and AMF promotes phosphorus utilization by stimulating rhizosphere microbial co-occurrence networks and lipid metabolites of Phragmites. Sci Total Environ, 2022, 845. ArticleID: 157339

[33] Li X, Du S, Hu S, Dong D, Jiang D, Cao C, Lin G, Fu J. Simulation of surface water–groundwater interaction in coal mining subsidence areas: A case study of the Kuye River Basin in China. J Hydrol, 2025, 659. ArticleID: 133243

[34] Liang J, Li Y, Si B, Wang Y, Chen X, Wang X, Chen H, Wang H, Zhang F, Bai Y, Biswas A. Optimizing biochar application to improve soil physical and hydraulic properties in saline-alkali soils. Sci Total Environ, 2021, 771. ArticleID: 144802

[35] Liang JF, An J, Gao JQ, Zhang XY, Song MH, Yu FH. Interactive effects of biochar and AMF on plant growth and greenhouse gas emissions from wetland microcosms. Geoderma, 2019, 346: 11-17.

[36] Liu H, Liang Y, Liu J, Zhang Q, Liu Y, Zeng J, Wang X, Yang G, Ren C, Han X. Long-term no-tillage enhanced soil multifunctionality and reduced microbial metabolic entropy. Appl Soil Ecol, 2025, 206. ArticleID: 105876

[37] Liu SY, Cao DY, Hang YW, Ge SH, He WY, Zhan ZY, He TY, Chen WF, Lan Y. Biochar affects the distribution of phosphorus in the soil profile by changing the capacity of soil to adsorb phosphorus and its distribution within soil macroaggregates. Land Degrad Dev, 2023, 34(8): 2189-2200.

[38] Ma X, Geng Q, Zhang H, Bian C, Chen HYH, Jiang D, Xu X. Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multifunctionality. New Phytol, 2021, 229: 2957-2969.

[39] Maestre FT, Guirado E, Armenteras D, Beck HE, AlShalan MS, Al-Saud NT, Chami R, Fu B, Gichenje H, Huber-Sannwald E, Speranza CI, Martínez-Valderrama J, McCabe MF, Orr B, Tang T, Metternicht G, Miess M, Reynolds JF, Stringer C, Wada Y, Duarte CM. Bending the curve of land degradation to achieve global environmental goals. Nature, 2025, 664: 347-355.

[40] Matinizadeh M, Nouri E, Bayranvand M, Kolarikova Z, Janousková M. Arbuscular mycorrhiza and rhizosphere soil enzymatic activities as modulated by grazing intensity and plant species identity in a semi-arid grassland. Rhizosphere, 2024, 30. ArticleID: 100893

[41] Mcgonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. A new method which gives an objective measure of colonization of roots byvesicular-arbuscular mycorrhizal fungi. New Phytol, 1990, 115(3): 495.

[42] Mikkelsen BL, Rosendahl S, Jakobsen I. Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol, 2008, 180(4): 890-898.

[43] Nguyen TB, Sherpa K, Bui XT, Nguyen VT, Vo TDH, Ho HTT, Chen CW, Dong CD. Biochar for soil remediation: a comprehensive review of current research on pollutant removal. Environ Pollut, 2023, 337. ArticleID: 122571

[44] Ohsowski BM, Dunfield K, Klironomos JN, Hart MM. Plant response to biochar, compost, and mycorrhizal fungal amendments in post-mine sandpits. Restor Ecol, 2018, 26(1): 63e-72.

[45] Pan X, Li Y, Zhang R, Tian D, Wang P, Song L, Quan Q, Chen C, Niu S, Zhang X, Wang J. Soil microbial gene abundance rather than diversity and network complexity predominantly determines soil multifunctionality in Tibetan alpine grasslands along a precipitation gradient. Funct Ecol, 2024, 38: 1210-1221.

[46] Pokharel P, Ma Z, Chang SX. Biochar increases soil microbial biomass with changes in extra-and intracellular enzyme activities: a global meta-analysis. Biochar, 2020, 2(1): 65-79.

[47] Qiao Y, Bai Y, She W, Liu L, Miao C, Zhu G, Qin S, Zhang Y. Arbuscular mycorrhizal fungi outcompete fine roots in determining soil multifunctionality and microbial diversity in a desert ecosystem. Appl Soil Ecol, 2022, 171. ArticleID: 104323

[48] Razzaghi F, Obour PB, Arthur E. Does biochar improve soil water retention? A systematic review and meta-analysis. Geoderma, 2020, 361. ArticleID: 114055

[49] Ren T, Liao J, Jin L, Delgado-Baquerizo M, Ruan H. Application of biogas-slurry and biochar improves soil multifunctionality in a poplar plantation during aforestation processes. Plant Soil, 2024, 501: 107-123.

[50] Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A. Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytolgist, 2015, 205: 1385-1388.

[51] Rosenthal J, Gunn KM. Arbuscular mycorrhizal fungi in biochar amended soils: a review. Soil Res, 2025, 63. ArticleID: SR24123

[52] Sonter LJ, Dade MC, Watson JE, Valent RK. Renewable energy production will exacerbate mining threats to biodiversity. Nat Commun, 2020, 11. ArticleID: 4174

[53] Sun J, Jia Q, Li Y, Zhang T, Chen J, Ren Y, Dong K, Xu S, Shi NN, Fu S. Effects of arbuscular mycorrhizal fungi and biochar on growth, nutrient absorption, and physiological properties of maize (Zea mays L.). J Fungi, 2022, 8. ArticleID: 1275

[54] Syakur S, Zaitun Z, Darusman D, Siagian GM. Improving the physical properties of ex-coal mining soil planted with sweet corn (Zea mays saccharata L.) using pine wood and sawdust biochar. Media Konservasi, 2024, 29(4): 540-549.

[55] Tang B, Man J, Lehmann A, Rillig M C. Arbuscular mycorrhizal fungi attenuate negative impact of drought on soil functions. Glob Change Biol, 2024, 30. ArticleID: e17409

[56] Thomopoulos S, Munkholm LJ, Elsgaard L, Ravnskov S. Tillage and residue management modulate the links between soil physical signatures and arbuscular mycorrhizal fungal biomarkers. Geoderma, 2025, 454. ArticleID: 117204

[57] Tuyishimire E, Cui J, Tang X, Sun Z, Cheng J. Interactive effects of honeysuckle planting and biochar amendment on soil structure and hydraulic properties of hillslope farmland. Agriculture, 2022, 12(3): 414.

[58] Van Der Heyde M, Bunce M, Dixon K, Wardell-Johnson G, White N, Nevill P. Changes in soil microbial communities in post mine ecological restoration: implications for monitoring using high throughput DNA sequencing. Sci Total Environ, 2020, 749. ArticleID: 142262

[59] Wang D, Fonte SJ, Parikh SJ, Six J, Scow KM. Biochar additions can enhance soil structure and the physical stabilization of C in aggregates. Geoderma, 2017, 303: 110-117.

[60] Wang PY, Zhao ZY, Siddique KHM, Xiong XB, Tao HY, Ma Y, Mo F, Chen YL, Song YJ, Burch JWR, Ma BL, Wang S, Kavagi L, Yang FK, Xiong YC. Microplastics positively mediate soil multifunctionality in dryland. Resour Conserv Recycl, 2024, 209. ArticleID: 107754

[61] Wang W, Dong Y, Wang HB, Xue DH, Zhang HF, Li ZJ, Wang H, Bo HJ, Zhang WJ, Zhang BH, Xiong YC, Zhang Q, Jin DS. Long-term legume cultivation affects the soil bacterial community via altering the soil pore structure in coal mine reclamation agroecosystems. Plant Cell Environ, 2025.

[62] Wang W, Dong Y, Zhang HF, Xue DH, Wang HB, Bo HJ, Xiong YC, He X, Zhang BH, Zhang WJ, Zhang Q, Xu MG, Jin DS. Leguminous crops as a nature-based strategy to restore the functionality of reclaimed soils in coal mine agroecosystem. Appl Soil Ecol, 2025, 214. ArticleID: 106407

[63] Wang YF, Chen P, Wang FH, Han WX, Qiao M, Dong WX, Hu CS, Zhu D, Chu HY, Zhu YG. The ecological clusters of soil organisms drive the ecosystem multifunctionality under long-term fertilization. Environ Int, 2022, 161. ArticleID: 107133

[64] Wen Z, Chen Y, Liu Z, Meng J. Biochar and arbuscular mycorrhizal fungi stimulate rice root growth strategy and soil nutrient availability. Eur J Soil Biol, 2022, 113. ArticleID: 103448

[65] Woolf D, Amonette JE, Street-Perrott FA, Lehmann J, Joseph S. Sustainable biochar to mitigate global climate change. Nat Commun, 2010, 1. ArticleID: 56

[66] Wu D, Senbayram M, Zang H, Ugurlar F, Aydemir S, Brüggemann N, Kuzyakov Y, Bol R, Blagodatskaya E. Effect of biochar origin and soil pH on greenhouse gas emissions from sandy and clay soils. Appl Soil Ecol, 2018, 129: 121-127.

[67] Wu QS, Wang S, Srivastava AK. Mycorrhizal hyphal disruption induces changes in plant growth, glomalin-related soil protein and soil aggregation of trifoliate orange in a core system. Soil Tillage Res, 2016, 160: 82-91.

[68] Xing XG, Liu Y, Ma XY. A modified van-Genuchten model for soil-water retention modeling by considering plant additives. Arch Agron Soil Sci, 2019, 65(4): 435-449.

[69] Xu R, Li J, Li X, Song W. Effect of coal mining subsidence on soil microbial communities in mining areas with high groundwater levels. Environ Geochem Health, 2025, 47(7): 245.

[70] Yang Q, Ravnskov S, Neumann Andersen M. Nutrient uptake and growth of potato: arbuscular mycorrhiza symbiosis interacts with quality and quantity of amended biochars. J Plant Nutr Soil Sci, 2020, 183(2): 220e-232.

[71] Yang YM, Naseer M, Zhu Y, Zhu SG, Wang S, Wang BZ, Wang J, Zhu H, Wang W, Tao HY, Xiong YC. Dual effects of nZVI on maize growth and water use are positively mediated by arbuscular mycorrhizal fungi via rhizosphere interactions. Environ Pollut, 2022, 308. ArticleID: 119661

[72] Zhang D, Sun J, Peng S, Wang Y, Hua Q, Wu P, Lin X. Paddy-upland rotation combined with manure application: An optimal strategy for enhancing soil multifunctionality. J Environ Manage, 2025, 373. ArticleID: 123788

[73] Zhang F, Liu M, Li Y, Che Y, Xiao Y. Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Sci Total Environ, 2019, 655: 1150-1158.

[74] Zhang L, Fan JQ, Ding XD, He XH, Zhang FS, Feng G. Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. Soil Biol Biochem, 2014, 74: 177-183.

[75] Zhou X, Ke T, Li S, Deng S, An X, Ma X, De Philippis R, Chen L. Induced biological soil crusts and soil properties varied between slope aspect, slope gradient and plant canopy in the Hobq Desert of China. CATENA, 2020, 190. ArticleID: 104559

[76] Zhu SG, Duan HX, Tao HY, Zhu L, Zhou R, Yang YM, Zhang XL, Wang WY, Zhu H, Zhang W, Wang RQ, Tao XP, Xiong YC. Arbuscular mycorrhiza changes plant facilitation patterns and increases resource use efficiency in intercropped annual plants. Appl Soil Ecol, 2023, 191. ArticleID: 105030

Funding

The Research Start-up Project of Shanxi Agricultural University for Recruited Talents(2023BQ120)

Merit-based Open Competition Project of Shanxi Major Science and Technology Special Program(202201140601028-4)

National Natural Science Foundation of China(32571953)

Open Project Funding Project of the Engineering Technology Innovation Center for Ecological Protection and Restoration of the Middle Reaches of the Yellow River, Ministry of Natural Resources(2025080)

Promotive Scientific Research Fund for New PhD Graduates working in Shanxi Province(SXBYKY2023038)

Youth Science and Technology Research Program of Shanxi Province Basic Research Program(202303021222077)

RIGHTS & PERMISSIONS

The Author(s)