Magnesium-doped biochars increase soil phosphorus availability by regulating phosphorus retention, microbial solubilization and mineralization

Abstract

Despite fertilization efforts, phosphorus (P) availability in soils remains a major constraint to global plant productivity. Soil incorporation of biochar could promote soil P availability but its effects remain uncertain. To attain further improvements in soil P availability with biochar, we developed, characterized, and evaluated magnesium-oxide (MgO) and sepiolite (Mg₄Si₆O₁₅(OH)₂·6H₂O)-functionalized biochars with optimized P retention/release capacity. Field-based application of these biochars for improving P availability and their mechanisms during three growth stages of maize was investigated. We further leveraged next-generation sequencing to unravel their impacts on the plant growth-stage shifts in soil functional genes regulating P availability. Results showed insignificant variation in P availability between single super phosphate fertilization (F) and its combination with raw biochar (BF). However, the occurrence of Mg-bound minerals on the optimized biochars’ surface adjusted its surface charges and properties and improved the retention and slow release of inorganic P. Compared to BF, available P (AP) was 26.5% and 19.1% higher during the 12-leaf stage and blister stage, respectively, under MgO-optimized biochar + F treatment (MgOBF), and 15.5% higher under sepiolite-biochar + F (SBF) during maize physiological maturity. Cumulatively, AP was 15.6% and 13.2% higher in MgOBF and SBF relative to BF. Hence, plant biomass, grain yield, and P uptake were highest in MgOBF and SBF, respectively at harvest. Optimized-biochar amendment stimulated microbial 16SrRNA gene diversity and suppressed the expression of P starvation response and P uptake and transport-related genes while stimulating P solubilization and mineralization genes. Thus, the optimized biochars promoted P availability via the combined processes of slow-release of retained phosphates, while inducing the microbial solubilization and mineralization of inorganic and organic P, respectively. Our study advances strategies for reducing cropland P limitation and reveals the potential of optimized biochars for improving P availability on the field scale.

Article Highlights

•	MgO and sepiolite doping optimized biochar’s surface properties for phosphorus (P) retention and slow release
•	The potential formation of Mg-PO4 phases on the optimized biochar surface regulated P retention and release
•	MgO and sepiolite-ptimized biochars increased soil available P by promoting microbial P mineralization and solubilization.

Keywords

Phosphorus limitation / Cropland / Functional genes / Field crops / Maize production

References

[1] Agegnehu G, Nelson PN, Bird MI. Crop yield, plant nutrient uptake and soil physicochemical properties under organic soil amendments and nitrogen fertilization on Nitisols. Soil till Res, 2016, 160: 1-13,

[2] Andersson H, Bergström L, Djodjic F, Ulén B, Kirchmann H. Topsoil and subsoil properties influence phosphorus leaching from four agricultural soils. J Environ Qual, 2013, 42: 455-463,

[3] Arif M, Ilyas M, Riaz M, Ali K, Shah K, Haq IU, Fahad S. Biochar improves phosphorus use efficiency of organic-inorganic fertilizers, maize-wheat productivity and soil quality in a low fertility alkaline soil. Field Crops Res, 2017, 214: 25-37,

[4] Bornø ML, Eduah JO, Müller-Stöver DS, Liu F. Effect of different biochars on phosphorus (P) dynamics in the rhizosphere of Zea mays L. (maize). Plant Soil, 2018, 431: 257-272,

[5] Bornø ML, Müller-Stöver DS, Liu F. Contrasting effects of biochar on phosphorus dynamics and bioavailability in different soil types. Sci Total Environ, 2018, 627: 963-974,

[6] Chan KY, Van Zwieten L, Meszaros I, Downie A, Joseph S. Agronomic values of greenwaste biochar as a soil amendment. Soil Res, 2007, 45: 629-634,

[7] Chen Q, Qin J, Cheng Z, Huang L, Sun P, Chen L, Shen G. Synthesis of a stable magnesium-impregnated biochar and its reduction of phosphorus leaching from soil. Chemosphere, 2018, 199: 402-408,

[8] Chintala R, Schumacher TE, McDonald LM, Clay DE, Malo DD, Papiernik SK, Clay SA, Julson JL. Phosphorus sorption and availability from biochars and soil/biochar mixtures. Clean–soil Air, Water, 2014, 42: 626-634,

[9] Chowdhury RB, Moore GA, Weatherley AJ, Arora M. Key sustainability challenges for the global phosphorus resource, their implications for global food security, and options for mitigation. J Clean Prod, 2017, 140: 945-963,

[10] Cui X, Dai X, Khan KY, Li T, Yang X, He Z. Removal of phosphate from aqueous solution using magnesium-alginate/chitosan modified biochar microspheres derived from Thalia dealbata. Biores Technol, 2016, 218: 1123-1132,

[11] Dai Z, Liu G, Chen H, Chen C, Wang J, Ai S, Wei D, Li D, Ma B, Tang C. Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. The ISME J, 2020, 14: 757-770,

[12] Deinert L, Hossen S, Ikoyi I, Kwapinksi W, Noll M, Schmalenberger A. Poultry litter biochar soil amendment affects microbial community structures, promotes phosphorus cycling and growth of barley (Hordeum vulgare). Europ J Soil Biol, 2024, 120,

[13] DeLuca TH, Gundale MJ, MacKenzie MD, Jones DL. Biochar effects on soil nutrient transformations. Biochar Environ Manag Sci Technol Implement, 2015, 2: 421-454,

[14] Dey S, Purakayastha TJ, Sarkar B, Rinklebe J, Kumar S, Chakraborty R, Datta A, Lal K, Shivay YS. Enhancing cation and anion exchange capacity of rice straw biochar by chemical modification for increased plant nutrient retention. Sci Total Environ, 2023, 886,

[500] Do Carmo Horta M, Torrent J. Phosphorus desorption kinetics in relation to phosphorus forms and sorption properties of Portuguese acid soils. Soil Sci, 2007, 172(8): 631-638,

[15] Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI. PICRUSt2 for prediction of metagenome functions. Nat Biotech, 2020, 38: 685-688,

[16] Eder S, Shi L, Jensen K, Yamane K, Hulett FM. A Bacillus subtilis secreted phosphodiesterase/alkaline phosphatase is the product of a Pho regulon gene, phoD. Microbiology, 1996, 142: 2041-2047,

[17] Elias MD, Tanaka M, Sakai M, Toyama H, Matsushita K, Adachi O, Yamada M. C-terminal periplasmic domain of Escherichia coli quinoprotein glucose dehydrogenase transfers electrons to ubiquinone. J Biol Chemist, 2001, 276: 48356-48361,

[18] Enders A, Lehmann J. Comparison of wet-digestion and dry-ashing methods for total elemental analysis of biochar. Commun Soil Sci Plant Anal, 2012, 43: 1042-1052,

[19] Frost RL, Cash GA, Kloprogge JT. Rocky Mountain leather', sepiolite and attapulgite—an infrared emission spectroscopic study. Vibrat Spectr, 1998, 16: 173-184,

[20] Gao S, DeLuca TH, Cleveland CC. Biochar additions alter phosphorus and nitrogen availability in agricultural ecosystems: a meta-analysis. Sci Total Environ, 2019, 654: 463-472,

[21] Glaser B, Lehr V-I. Biochar effects on phosphorus availability in agricultural soils: a meta-analysis. Scien Rep, 2019, 9: 9338,

[22] Helfenstein J, Tamburini F, von Sperber C, Massey MS, Pistocchi C, Chadwick OA, Vitousek PM, Kretzschmar R, Frossard E. Combining spectroscopic and isotopic techniques gives a dynamic view of phosphorus cycling in soil. Nat Comm, 2018, 9: 3226,

[23] Hornak J. Synthesis, properties, and selected technical applications of magnesium oxide nanoparticles: a review. Int J Mol Sci, 2021, 22(23): 12752,

[24] Hou E, Luo Y, Kuang Y, Chen C, Lu X, Jiang L, Luo X, Wen D. Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat Comm, 2020, 11: 637,

[25] Hou E, Wen D, Jiang L, Luo X, Kuang Y, Lu X, Chen C, Allen KT, He X, Huang X. Latitudinal patterns of terrestrial phosphorus limitation over the globe. Ecol Lett, 2021, 24: 1420-1431,

[26] Hu W, Zhang Y, Xiangmin R, Fei J, Peng J, Luo G. Coupling amendment of biochar and organic fertilizers increases maize yield and phosphorus uptake by regulating soil phosphatase activity and phosphorus-acquiring microbiota. Agric, Ecosys Environ, 2023, 355,

[27] Ibrahim MM, Hu K, Tong C, Xing S, Zou S, Mao Y. De-ashed biochar enhances nitrogen retention in manured soil and changes soil microbial dynamics. Geoderma, 2020,

[28] Ibrahim MM, Tong C, Hu K, Zhou B, Xing S, Mao Y. Biochar-fertilizer interaction modifies N-sorption, enzyme activities and microbial functional abundance regulating nitrogen retention in rhizosphere soil. Sci Total Environ, 2020, 739,

[29] Ibrahim MM, Guo L, Wu F, Liu D, Zhang H, Zou S, Xing S, Mao Y. Field-applied biochar-based MgO and sepiolite composites possess CO2 capture potential and alter organic C mineralization and C-cycling bacterial structure in fertilized soils. Sci Total Environ, 2022, 813,

[30] Ibrahim MM, Liu D, Wu F, Chen Y, He Z, Zhang W, Xing S, Mao Y. Nitrogen retention potentials of magnesium oxide-and sepiolite-modified biochars and their impacts on bacterial distribution under nitrogen fertilization. Sci Total Environ, 2023, 866,

[31] Ibrahim MM, Wu F, Chen Y, Liu D, Zhang W, He Z, Hou E, Xing S, Mao Y. Impacts of MgO-and sepiolite-biochar composites on N-partitioning and dynamics of N-cycling bacteria in a soil-maize system: a field-based 15N-urea tracer study. Geoderma, 2023, 429,

[32] Ishfaq M, Wang Y, Yan M, Wang Z, Wu L, Li C, Li X. Physiological essence of magnesium in plants and its widespread deficiency in the farming system of China. Front Plant Sci, 2022, 13,

[33] Jin J, Fang Y, He S, Liu Y, Liu C, Li F, Khan S, Eltohamy KM, Liu B, Liang X. Improved phosphorus availability and reduced degree of phosphorus saturation by biochar-blended organic fertilizer addition to agricultural field soils. Chemosphere, 2023, 317,

[34] Jin J, Khan S, Eltohamy KM, He S, Liu C, Li F, Liang X. Biochar–coupled organic fertilizer reduced soil water-dispersible colloidal phosphorus contents in agricultural fields. Chemosphere, 2023, 333,

[35] Kahura MW, Min H-G, Kim M-S, Kim J-G. Assessing phosphorus availability in a high pH, biochar amended soil under inorganic and organic fertilization. Ecol Resil Infrastr, 2018, 5: 11-18,

[36] Kehler A, Haygarth P, Tamburini F, Blackwell M. Cycling of reduced phosphorus compounds in soil and potential impacts of climate change. European J Soil Sci, 2021, 72: 2517-2537,

[37] Khan MI, Afzal MJ, Bashir S, Naveed M, Anum S, Cheema SA, Wakeel A, Sanaullah M, Ali MH, Chen Z. Improving nutrient uptake, growth, yield and protein content in chickpea by the co-addition of phosphorus fertilizers, organic manures, and Bacillus sp. MN-54. Agronomy, 2021, 11: 436,

[38] Lalley J, Han C, Li X, Dionysiou DD, Nadagouda MN. Phosphate adsorption using modified iron oxide-based sorbents in lake water: kinetics, equilibrium, and column tests. Chem Eng J, 2016, 284: 1386-1396,

[39] Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D. Biochar effects on soil biota–a review. Soil Biol Biochem, 2011, 43: 1812-1836,

[40] Li X, Rui J, Mao Y, Yannarell A, Mackie R. Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem, 2014, 68: 392-401,

[41] Li R, Wang JJ, Zhou B, Zhang Z, Liu S, Lei S, Xiao R. Simultaneous capture removal of phosphate, ammonium and organic substances by MgO impregnated biochar and its potential use in swine wastewater treatment. J Clean Prod, 2017, 147: 96-107,

[42] Liu J, Sui P, Cade-Menun BJ, Hu Y, Yang J, Huang S, Ma Y. Molecular-level understanding of phosphorus transformation with long-term phosphorus addition and depletion in an alkaline soil. Geoderma, 2019, 353: 116-124,

[43] Liu Z, Wu Z, Tian F, Liu X, Li T, He Y, Li B, Zhang Z, Yu B. Phosphate-solubilizing microorganisms regulate the release and transformation of phosphorus in biochar-based slow-release fertilizer. Sci Total Environ, 2023, 869,

[44] Lu J, Li Y, Cai Y, Jiang P, Yu B. Co-incorporation of hydrotalcite and starch into biochar-based fertilizers for the synthesis of slow-release fertilizers with improved water retention. Biochar, 2023, 5: 44,

[45] Luo S, Wang S, Tian L, Li S, Li X, Shen Y, Tian C. Long-term biochar application influences soil microbial community and its potential roles in semiarid farmland. Appl Soil Ecol, 2017, 117: 10-15,

[46] Marschner P (2012) Marschner's mineral nutrition of higher plants (3rd ed.). Academic Press. https://doi.org/10.1016/C2009-0-63043-9

[47] Mohammadi N, Shariatmadari H, Khademi H, Bazarganipour M. Coating of sepiolite-chitosan nanocomposites onto urea increases nitrogen availability and its use efficiency in maize. Arch Agron Soil Sci, 2020, 66: 884-896,

[48] Palansooriya KN, Wong JTF, Hashimoto Y, Huang L, Rinklebe J, Chang SX, Bolan N, Wang H, Ok YS. Response of microbial communities to biochar-amended soils: a critical review. Biochar, 2019, 1: 3-22,

[49] Penn CJ, Camberato JJ. A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture, 2019, 9: 120,

[50] Qayyum MF, Haider G, Iqbal M, Hameed S, Ahmad N, Rehman MZu, Majeed A, Rizwan M, Ali S. Effect of alkaline and chemically engineered biochar on soil properties and phosphorus bioavailability in maize. Chemosphere, 2021, 266,

[51] Rafique M, Ortas I, Rizwan M, Chaudhary HJ, Gurmani AR, Munis MFH. Residual effects of biochar and phosphorus on growth and nutrient accumulation by maize (Zea mays L.) amended with microbes in texturally different soils. Chemosphere, 2020, 238,

[52] Richardson AE, Simpson RJ. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol, 2011, 156: 989-996,

[53] Sarfraz R, Yang W, Wang S, Zhou B, Xing S. Short term effects of biochar with different particle sizes on phosphorous availability and microbial communities. Chemosphere, 2020, 256,

[54] Shi W, Ju Y, Bian R, Li L, Joseph S, Mitchell DRG, Munroe P, Taherymoosavi S, Pan G. Biochar bound urea boosts plant growth and reduces nitrogen leaching. Sci Total Environ, 2020, 701,

[55] Shi Y, Yu Y, Chang E, Wang R, Hong Z, Cui J, Zhang F, Jiang J, Xu R. Effect of biochar incorporation on phosphorus supplementation and availability in soil: a review. J Soil Sedim, 2023, 23: 672-686,

[56] Song D, Tang J, Xi X, Zhang S, Liang G, Zhou W, Wang X. Responses of soil nutrients and microbial activities to additions of maize straw biochar and chemical fertilization in a calcareous soil. Europ J Soil Biol, 2018, 84: 1-10,

[57] Streubel JD, Collins HP, Tarara JM, Cochran RL. Biochar produced from anaerobically digested fiber reduces phosphorus in dairy lagoons. J Environ Qual, 2012, 41: 1166-1174,

[58] Sun K, Qiu M, Han L, Jin J, Wang Z, Pan Z, Xing B. Speciation of phosphorus in plant-and manure-derived biochars and its dissolution under various aqueous conditions. Sci Total Environ, 2018, 634: 1300-1307,

[59] Tan X-F, Liu Y-G, Gu Y-l, Xu Y, Zeng G-M, Hu X-J, Liu S-B, Wang X, Liu S-M, Li J. Biochar-based nano-composites for the decontamination of wastewater: a review. Bioresource Technol, 2016, 212: 318-333,

[60] Tao Q, Li B, Li Q, Han X, Jiang Y, Jupa R, Wang C, Li T. Simultaneous remediation of sediments contaminated with sulfamethoxazole and cadmium using magnesium-modified biochar derived from Thalia dealbata. Sci Total Environ, 2019, 659: 1448-1456,

[61] Tian J, Wang J, Dippold M, Gao Y, Blagodatskaya E, Kuzyakov Y. Biochar affects soil organic matter cycling and microbial functions but does not alter microbial community structure in a paddy soil. Sci Total Environ, 2016, 556: 89-97,

[62] Tian XY, He DD, Bai S, et al.. Physiological and molecular advances in magnesium nutrition of plants. Plant Soil, 2021, 468: 1-17,

[63] Vitousek PM, Naylor R, Crews T, David MB, Drinkwater LE, Holland E, Johnes PJ, Katzenberger J, Martinelli LA, Matson PA. Nutrient imbalances in agricultural development. Science, 2009, 324: 1519-1520,

[64] Wan W, Hao X, Xing Y, Liu S, Zhang X, Li X, Chen W, Huang Q. Spatial differences in soil microbial diversity caused by pH-driven organic phosphorus mineralization. Land Degrada Devel, 2021, 32: 766-776,

[65] Willey JM, Sherwood LM, Woolverton CJ. . Prescott's microbiology, 2014 New York McGraw-Hill

[66] Wu L, Wei C, Zhang S, Wang Y, Kuzyakov Y, Ding X. MgO-modified biochar increases phosphate retention and rice yields in saline-alkaline soil. J Clean Prod, 2019, 235: 901-909,

[67] Xiong J, Zhou M, Qu C, Yu D, Chen C, Wang M, Tan W. Quantitative analysis of Pb adsorption on sulfhydryl-modified biochar. Biochar, 2021, 3: 37-49,

[68] Xu G, Zhang Y, Sun J, Shao H. Negative interactive effects between biochar and phosphorus fertilization on phosphorus availability and plant yield in saline sodic soil. Sci Total Environ, 2016, 568: 910-915,

[69] Yang X, Wan Y, Zheng Y, He F, Yu Z, Huang J, Wang H, Ok YS, Jiang Y, Gao B. Surface functional groups of carbon-based adsorbents and their roles in the removal of heavy metals from aqueous solutions: a critical review. Chem Eng J, 2019, 366: 608-621,

[501] Yao Y, Gao B, Inyang M, Zimmerman AR, Cao X, Pullammanappallil P, Yang L. (2011) Removal of phosphate from aqueous solution by biochar derived from anaerobically digested sugar beet tailings. J Hazard Mater 190(1-3), 501–507. https://doi.org/10.1016/j.jhazmat.2011.03.083

[70] Yao Y, Gao B, Chen J, Yang L. Engineered biochar reclaiming phosphate from aqueous solutions: mechanisms and potential application as a slow-release fertilizer. Environ Sci Technol, 2013, 47: 8700-8708,

[71] Yin X, Xu Y, Huang R, Huang Q, Xie Z, Cai Y, Liang X. Remediation mechanisms for Cd-contaminated soil using natural sepiolite at the field scale. Environ Sci Process Impacts, 2017, 19: 1563-1570,

[72] Yin Q, Wang R, Zhao Z. Application of Mg–Al-modified biochar for simultaneous removal of ammonium, nitrate, and phosphate from eutrophic water. J Clean Prod, 2018, 176: 230-240,

[73] Zhan F, Zeng W, Yuan X, Li B, Li T, Zu Y, Jiang M, Li Y. Field experiment on the effects of sepiolite and biochar on the remediation of Cd-and Pb-polluted farmlands around a Pb–Zn mine in Yunnan Province, China. Environ Sci Poll Res, 2019, 26: 7743-7751,

[74] Zhang M, Gao B, Yao Y, Xue Y, Inyang M. Synthesis of porous MgO-biochar nano-composites for removal of phosphate and nitrate from aqueous solutions. Chem Eng J, 2012, 210: 26-32,

[75] Zhang H, Chen C, Gray EM, Boyd SE, Yang H, Zhang D. Roles of biochar in improving phosphorus availability in soils: a phosphate adsorbent and a source of available phosphorus. Geoderma, 2016, 276: 1-6,

[76] Zhang Y, Wang J, Feng Y. The effects of biochar addition on soil physicochemical properties: a review. CATENA, 2021, 202,

[77] Zhao Z, Ibrahim MM, Wang X, Xing S, Heiling M, Hood-Nowotny R, Tong C, Mao Y. Properties of biochar derived from spent mushroom substrates. BioResources, 2019, 14: 5254-5277,

[78] Zheng Y, Wan Y, Chen J, Chen H, Gao B. MgO modified biochar produced through ball milling: a dual-functional adsorbent for removal of different contaminants. Chemosphere, 2020, 243,

[79] Zhou F, Ye G, Gao Y, Wang H, Zhou S, Liu Y, Yan C. Cadmium adsorption by thermal-activated sepiolite: application to in-situ remediation of artificially contaminated soil. J Hazard Mater, 2022, 423,

[80] Zhu J, Li M, Whelan M. Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ, 2018, 612: 522-537,

[81] Zwetsloot MJ, Lehmann J, Bauerle T, Vanek S, Hestrin R, Nigussie A. Phosphorus availability from bone char in a P-fixing soil influenced by root-mycorrhizae-biochar interactions. Plant Soil, 2016, 408: 95-105,

Funding

Basic and Applied Basic Research Foundation of Guangdong Province(2022B1515020014); China Postdoctoral Science Foundation(2023M743544); Fujian Forestry and Technology Promotion Project(2020TG17); University-Industry Cooperation Project of Fujian Province(2021N5002)