Short-term microbial community dynamics induced by ¹³C-labeled maize root, its derived biochar and NPK in long-term amended soil

Abstract

Crop residues and their derived biochar are frequently used for their potential to improve grain yield, soil fertility and carbon (C) sequestration. However, the effects of root are often overlooked, and the effects of chemical fertilizer (NPK) combined with root or its biochar on microbial community structure need further study. This study used ¹³C-labeled maize root, its biochar and soil with different fertilization for 8 years as materials and substrates. A 112-day incubation experiment was conducted to explore the effects of microbial community on the C processing. During incubation, the root-C (54.9%) mineralized significantly more than biochar-C (12.8%), while NPK addition significantly increased the root-C mineralization. Adding biochar alone did not significantly change the microbial community. Compared to the biochar treatment (BC), the root treatment (R) notably increased the contents of total phospholipid fatty acids (PLFAs), ¹³C-PLFA and the proportion of fungi and Gram-negative bacteria, but reduced the proportion of actinomycetes. The root mineralization was significantly correlated with the relative content of ¹³C-Gram-positive bacteria and ¹³C-fungi, while biochar mineralization was significantly correlated with the relative content of ¹³C-Gram-positive bacteria and ¹³C-actinomycetes. Notably, NPK addition significantly increased the contribution of biochar-C to PLFA-C pool, while decreasing the contribution of root-C. In summary, due to microbial adaptation to the lack of bioavailable C in biochar-amended soil, biochar can act as a buffer against the significant disturbance caused by NPK to microbial communities and native soil organic carbon (SOC), which contributes to the steady enhancement in soil C storage.

Highlights

•	The addition of biochar alone for 8 consecutive years did not change the composition of the microbial community structure, but the total PLFA content increased significantly compared to the control.
•	NPK addition reduced the proportion of microbial assimilation of root-C, while increasing the proportion of microbial assimilation of biochar-C.
•	The effect of NPK on microbial biomass is short-lived, but the effect on microbial community structure is long-lasting.
•	Biochar has a stronger buffering effect on the drastic changes in microbial communities and native SOC caused by NPK.

Keywords

Biochar / Maize root / ¹³C-PLFA / Microbial community structure / NPK

References

[1] Abiven S, Recous S, Reyes V, Oliver R. Mineralisation of C and N from root, stem and leaf residues in soil and role of their biochemical quality. Biol Fertil Soils, 2005, 42: 119-128,

[2] Acosta-Martínez V, Dowd SE, Sun Y, Allen VGJSB. Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem, 2008, 40: 2762-2770,

[3] Andresen LC, Dungait JAJ, Bol R, Selsted MB, Ambus P, Michelsen A. Bacteria and fungi respond differently to multifactorial climate change in a temperate heathland, traced with 13C-glycine and FACE CO2. PLoS One, 2014, 9: e85070,

[4] Arcand MM, Helgason BL, Lemke RL. Microbial crop residue decomposition dynamics in organic and conventionally managed soils. Appl Soil Ecol, 2016, 107: 347-359,

[5] Atkinson CJ, Fitzgerald JD, Hipps NA. Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant Soil, 2010, 337: 1-18,

[6] Awad YM, Ok YS, Abrigata J, Beiyuan JZ, Beckers F, Tsang DCW, Rinklebe J. Pine sawdust biomass and biochars at different pyrolysis temperatures change soil redox processes. Sci Total Environ, 2018, 625: 147-154,

[7] Azeem M, Sun D, Crowley DE, Hayat R, Hussain Q, Ali A, Tahir MI, Jeyasundar PGSA, Rinklebe J, Zhang Z. Crop types have stronger effects on soil microbial communities and functionalities than biochar or fertilizer during two cycles of legume-cereal rotations of dry land. Sci Total Environ, 2020, 715,

[8] Bai Z, Liang C, Bode S, Huygens D, Boeckx P. Phospholipid C-13 stable isotopic probing during decomposition of wheat residues. Appl Soil Ecol, 2016, 98: 65-74,

[9] Bei Q, Liu G, Tang H, Cadisch G, Rasche F, Xie Z. Heterotrophic and phototrophic 15 N 2 fixation and distribution of fixed 15 N in a flooded rice–soil system. Soil Biol Biochem, 2013, 59: 25-31,

[10] Blagodatskaya E, Kuzyakov Y. Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem, 2013, 67: 192-211,

[11] Bossio DA, Cook-Patton SC, Ellis PW, Fargione JE, Sanderman J, Smith P, Wood SU, Zomer RJ, Von Unger M, Emmer IM, Griscom BW. The role of soil carbon in natural climate solutions. Nat Sustain, 2020, 3: 391-398,

[12] Bowen SR (2006) Biologically relevant characteristics of dissolved organic carbon (DOC) from soil. Ph.D. thesis, Univ. of Stirling, Stirling, U. K

[13] Brant JB, Sulzman EW, Myrold DD. Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol Biochem, 2006, 38: 2219-2232,

[14] Carrara JE, Walter CA, Freedman ZB, Hostetler AN, Hawkins JS, Fernandez IJ, Brzostek ER. Differences in microbial community response to nitrogen fertilization result in unique enzyme shifts between arbuscular and ectomycorrhizal-dominated soils. Global Change Biol, 2021, 27: 2049-2060,

[15] Chen J, Li S, Liang C, Xu Q, Li Y, Qin H, Fuhrmann JJ. Response of microbial community structure and function to short-term biochar amendment in an intensively managed bamboo (Phyllostachys praecox) plantation soil: effect of particle size and addition rate. Sci Total Environ, 2017, 574: 24-33,

[16] Chen W, Meng J, Han X, Lan Y, Zhang W. Past, present, and future of biochar. Biochar, 2019, 1: 75-87,

[17] Chen Q, Niu B, Hu Y, Wang J, Lei T, Xu-Ri ZJ, Xi C, Zhang G. Multilevel nitrogen additions alter chemical composition and turnover of the labile fraction soil organic matter via effects on vegetation and microorganisms. J Geophys Res-Biogeo, 2020, 125: e2019JG005316,

[18] Dai Z, Xiong X, Zhu H, Xu H, Leng P, Li J, Tang C, Xu J. Association of biochar properties with changes in soil bacterial, fungal and fauna communities and nutrient cycling processes. Biochar, 2021, 3: 239-254,

[19] Dangi S, Gao S, Duan Y, Wang D. Soil microbial community structure affected by biochar and fertilizer sources. Appl Soil Ecol, 2020, 150: 103452,

[20] De Deyn GB, Quirk H, Oakley S, Ostle N, Bardgett RD. Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences, 2011, 8: 1131-1139,

[21] Dungait JAJ, Kemmitt SJ, Michallon L, Guo S, Wen Q, Brookes PC, Evershed RP. Variable responses of the soil microbial biomass to trace concentrations of 13C-labelled glucose, using 13C-PLFA analysis. Eur J Soil Sci, 2010, 62: 117-126,

[22] Dungait JAJ, Hopkins DW, Gregory AS, Whitmore AP. Soil organic matter turnover is governed by accessibility not recalcitrance. Global Change Biol, 2012, 18: 1781-1796,

[23] Farrell M, Kuhn TK, Macdonald LM, Maddern TM, Murphy DV, Hall PA, Singh BP, Baumann K, Krull ES, Baldock JA. Microbial utilisation of biochar-derived carbon. Sci Total Environ, 2013, 465: 288-297,

[24] Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology, 2007, 88: 1354-1364,

[25] Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA. Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem, 2011, 43: 86-96,

[26] Ge T, Li B, Zhu Z, Hu Y, Yuan H, Dorodnikov M, Jones DL, Wu J, Kuzyakov Y. Rice rhizodeposition and its utilization by microbial groups depends on N fertilization. Biol Fertil Soils, 2016, 53: 37-48,

[27] Genre A, Lanfranco L, Perotto S, Bonfante P. Unique and common traits in mycorrhizal symbioses. Nat Rev Microbiol, 2020, 18: 649-660,

[28] Gomez JD, Denef K, Stewart CE, Zheng J, Cotrufo MF. Biochar addition rate influences soil microbial abundance and activity in temperate soils. Eur J Soil Sci, 2014, 65: 28-39,

[29] Gul S, Whalen JK, Thomas BW, Sachdeva V, Deng H. Physico-chemical properties and microbial responses in biochar-amended soils: mechanisms and future directions. Agr Ecosyst Environ, 2015, 206: 46-59,

[30] Hamer U, Unger M, Makeschin F. Impact of air-drying and rewetting on PLFA profiles of soil microbial communities. J Plant Nutr Soil Sci, 2007, 170: 259-264,

[31] Han L, Sun K, Jin J, Xing B. Some concepts of soil organic carbon characteristics and mineral interaction from a review of literature. Soil Biol Biochem, 2016, 94: 107-121,

[32] Helfrich M, Ludwig B, Thoms C, Gleixner G, Flessa H. The role of soil fungi and bacteria in plant litter decomposition and macroaggregate formation determined using phospholipid fatty acids. Appl Soil Ecol, 2015, 96: 261-264,

[33] Huang Y, Kudo S, Masek O, Norinaga K, Hayashi J-I. Simultaneous maximization of the char yield and volatility of oil from biomass pyrolysis. Energ Fuel, 2013, 27: 247-254,

[34] Ibrahim MM, Tong CX, Hu K, Zhou BQ, Xing SH, Mao YL. Biochar-fertilizer interaction modifies N-sorption, enzyme activities and microbial functional abundance regulating nitrogen retention in rhizosphere soil. Sci Total Environ, 2020, 739,

[35] Ippolito JA, Stromberger ME, Lentz RD, Dungan RS. Hardwood biochar influences calcareous soil physicochemical and microbiological status. J Environ Qual, 2014, 43: 681-689,

[36] Jones DL, Rousk J, Edwards-Jones G, Deluca TH, Murphy DV. Biochar-mediated changes in soil quality and plant growth in a three year field trial. Soil Biol Biochem, 2012, 45: 113-124,

[37] Keiluweit M, Nico PS, Johnson MG, Kleber M. Dynamic molecular structure of plant biomass-derived black carbon (biochar). Environ Sci Technol, 2010, 44: 1247-1253,

[38] Khan S, Waqas M, Ding F, Shamshad I, Arp HPH, Li G. The influence of various biochars on the bioaccessibility and bioaccumulation of PAHs and potentially toxic elements to turnips (Brassica rapa L.). J Hazard Mater, 2015, 300: 243-253,

[39] Kramer C, Gleixner G. Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biol Biochem, 2008, 40: 425-433,

[40] Kramer S, Dibbern D, Moll J, Huenninghaus M, Koller R, Krueger D, Marhan S, Urich T, Wubet T, Bonkowski M, Buscot F, Lueders T, Kandeler E. Resource partitioning between bacteria, fungi, and protists in the detritusphere of an agricultural soil. Front Microbiol, 2016, 7: 1524,

[41] Kuzyakov Y. Priming effects: Interactions between living and dead organic matter. Soil Biol Biochem, 2010, 42: 1363-1371,

[42] 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,

[43] Li F, Chen L, Zhang J, Yin J, Huang S. Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Front Microbiol, 2017, 8: 187,

[44] Li D, Li Z, Zhao B, Zhang J. Relationship between the chemical structure of straw and composition of main microbial groups during the decomposition of wheat and maize straws as affected by soil texture. Biol Fertil Soils, 2019, 56: 11-24,

[45] Li Z, Song M, Li D, Ma L, Zhao B, Zhang J. Effect of long-term fertilization on decomposition of crop residues and their incorporation into microbial communities of 6-year stored soils. Biol Fertil Soils, 2019, 56: 25-37,

[46] Li SL, Wang S, Fan MC, Wu Y, Shangguan ZP. Interactions between biochar and nitrogen impact soil carbon mineralization and the microbial community. Soil Till Res, 2020, 196,

[47] Liang C, Schimel JP, Jastrow JD. The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol, 2017, 2: 17105,

[48] Liu Z, Zhu M, Wang J, Liu X, Guo W, Zheng J, Bian R, Wang G, Zhang X, Cheng K, Liu X, Li L, Pan G. The responses of soil organic carbon mineralization and microbial communities to fresh and aged biochar soil amendments. GCB Bioenergy, 2019, 11: 1408-1420,

[49] Liu Q, Wu C, Wei L, Wang S, Deng Y, Ling W, Xiang W, Kuzyakov Y, Zhu Z, Ge T. Microbial mechanisms of organic matter mineralization induced by straw in biochar-amended paddy soil. Biochar, 2024, 6: 18,

[50] Mitchell PJ, Simpson AJ, Soong R, Simpson MJ. Shifts in microbial community and water-extractable organic matter composition with biochar amendment in a temperate forest soil. Soil Biol Biochem, 2015, 81: 244-254,

[51] Moore-Kucera J, Dick RP. Application of 13C-labeled litter and root materials for in situ decomposition studies using phospholipid fatty acids. Soil Biol Biochem, 2008, 40: 2485-2493,

[52] Müller K, Marhan S, Kandeler E, Poll C. Carbon flow from litter through soil microorganisms: from incorporation rates to mean residence times in bacteria and fungi. Soil Biol Biochem, 2017, 115: 187-196,

[53] Nilsson RH, Anslan S, Bahram M, Wurzbacher C, Baldrian P, Tedersoo L. Mycobiome diversity: high-throughput sequencing and identification of fungi. Nat Rev Microbiol, 2018, 17: 95-109,

[54] Olsson Pål Axel. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol, 1999, 29: 303-310,

[55] Oneill B, Grossman JM, Grossman JM, Tsai M-T, Gomes J, Lehmann J, Peterson J, Neves EG, Thies JE. Bacterial community composition in brazilian anthrosols and adjacent soils characterized using culturing and molecular identification. Microb Ecol, 2009, 58: 23-35,

[56] Pan F, Li Y, Chapman SJ, Yao H. Effect of rice straw application on microbial community and activity in paddy soil under different water status. Environ Sci Pollut R, 2016, 23: 5941-5948,

[57] Pan FX, Li YY, Chapman SJ, Khan S, Yao HY. Microbial utilization of rice straw and its derived biochar in a paddy soil. Sci Total Environ, 2016, 559: 15-23,

[58] Pang ZQ, Huang JW, Fallah N, Lin WX, Yuan ZN, Hu CH. Combining N fertilization with biochar affects root-shoot growth, rhizosphere soil properties and bacterial communities under sugarcane monocropping. Ind Crop Prod, 2022, 182: 114899,

[59] Paterson E, Sim A. Soil-specific response functions of organic matter mineralization to the availability of labile carbon. Global Change Biol, 2013, 19: 1562-1571,

[60] Potthast K, Hamer U, Makeschin F. Impact of litter quality on mineralization processes in managed and abandoned pasture soils in Southern Ecuador. Soil Biol Biochem, 2010, 42: 56-64,

[61] Powlson DS, Whitmore AP, Goulding KWT. Soil carbon sequestration to mitigate climate change: a critical re-examination to identify the true and the false. Eur J Soil Sci, 2011, 62: 42-55,

[62] Puget P, Drinkwater LE. Short-term dynamics of root- and shoot-derived carbon from a leguminous green manure. Soil Sci Soc Am J, 2001, 65: 771-779,

[63] Santos F, Torn MS, Bird JA. Biological degradation of pyrogenic organic matter in temperate forest soils. Soil Biol Biochem, 2012, 51: 115-124,

[64] Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology, 2007, 88: 1386-1394,

[65] Schmatz R, Recous S, Aita C, Tahir MM, Schu AL, Chaves B, Giacomini SJ. Crop residue quality and soil type influence the priming effect but not the fate of crop residue C. Plant Soil, 2016, 414: 229-245,

[66] Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE. Persistence of soil organic matter as an ecosystem property. Nature, 2011, 478: 49-56,

[67] Singh H, Northup BK, Rice CW, Prasad PVV. Biochar applications influence soil physical and chemical properties, microbial diversity, and crop productivity: a meta-analysis. Biochar, 2022, 4: 8,

[68] Smith JL, Collins HP, Bailey VL. The effect of young biochar on soil respiration. Soil Biol Biochem, 2010, 42: 2345-2347,

[69] Song DL, Chen L, Zhang S, Zheng Q, Ullah SM, Zhou W, Wang XB. Combined biochar and nitrogen fertilizer change soil enzyme and microbial activities in a 2-year field trial. Eur J Soil Biol, 2020, 99,

[70] Stewart CE, Zheng JY, Botte J, Cotrufo MF. Co-generated fast pyrolysis biochar mitigates green-house gas emissions and increases carbon sequestration in temperate soils. GCB Bioenergy, 2013, 5: 153-164,

[71] Strickland MS, Rousk J. Considering fungal:bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem, 2010, 42: 1385-1395,

[72] Terrer C, Phillips RP, Hungate BA, Rosende J, Pett-Ridge J, Craig ME, Van Groenigen KJ, Keenan TF, Sulman BN, Stocker BD, Reich PB, Pellegrini AFA, Pendall E, Zhang H, Evans RD, Carrillo Y, Fisher JB, Van Sundert K, Vicca S, Jackson RB. A trade-off between plant and soil carbon storage under elevated CO2. Nature, 2021, 591: 599,

[73] Theuerl S, Buscot F. Laccases: toward disentangling their diversity and functions in relation to soil organic matter cycling. Biol Fertil Soils, 2010, 46: 215-225,

[74] 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,

[75] Waldrop MP, Firestone MK. Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia, 2004, 138: 275-284,

[76] Wang J, Xiong Z, Kuzyakov Y. Biochar stability in soil: meta-analysis of decomposition and priming effects. GCB Bioenergy, 2015, 8: 512-523,

[77] Wang X, Song D, Liang G, Zhang Q, Ai C, Zhou W. Maize biochar addition rate influences soil enzyme activity and microbial community composition in a fluvo-aquic soil. Appl Soil Ecol, 2015, 96: 265-272,

[78] Wang Y, Zhao X, Guo Z, Jia Z, Wang S, Ding K. Response of soil microbes to a reduction in phosphorus fertilizer in rice-wheat rotation paddy soils with varying soil P levels. Soil Till Res, 2018, 181: 127-135,

[79] Waqas M, Khan S, Qing H, Reid BJ, Chao C. The effects of sewage sludge and sewage sludge biochar on PAHs and potentially toxic element bioaccumulation in Cucumis sativa L. Chemosphere, 2014, 105: 53-61,

[80] Watzinger A, Feichtmair S, Kitzler B, Zehetner F, Kloss S, Wimmer B, Zechmeister-Boltenstern S, Soja G. Soil microbial communities responded to biochar application in temperate soils and slowly metabolized ¹³C-labelled biochar as revealed by ¹³C PLFA analyses: results from a short-term incubation and pot experiment. Eur J Soil Sci, 2013, 65: 40-51,

[81] Xu Y, Sun L, Lal R, Bol R, Wang Y, Gao X, Ding F, Liang S, Li S, Wang J. Microbial assimilation dynamics differs but total mineralization from added root and shoot residues is similar in agricultural Alfisols. Soil Biol Biochem, 2020, 148: 107901,

[82] Yang CD, Liu JJ, Ying HC, Lu SG. Soil pore structure changes induced by biochar affect microbial diversity and community structure in an Ultisol. Soil Till Res, 2022, 224: 105505,

[83] Yuan MS, Zhu XZ, Sun HR, Song JR, Li C, Shen YF, Li SQ. The addition of biochar and nitrogen alters the microbial community and their cooccurrence network by affecting soil properties. Chemosphere, 2023, 312,

[84] Zelles L. Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils, 1999, 29: 111-129,

[85] Zhang P, Scheu S, Li B, Lin GH, Zhao JY, Wu JH. Litter C transformations of invasive Spartina alterniflora affected by litter type and soil source. Biol Fertil Soils, 2020, 56: 369-379,

[86] Zhang MY, Zhang L, Riaz M, Xia H, Jiang CC. Biochar amendment improved fruit quality and soil properties and microbial communities at different depths in citrus production. J Clean Prod, 2021, 292,

[87] Zheng JF, Chen JH, Pan GX, Liu XY, Zhang XH, Li LQ, Sian RJ, Cheng K, Jinweizheng Z. Biochar decreased microbial metabolic quotient and shifted community composition four years after a single incorporation in a slightly acid rice paddy from southwest China. Sci Total Environ, 2016, 571: 206-217,

[88] Zornoza R, Moreno-Barriga F, Acosta JA, Muñoz MA, Faz A. Stability, nutrient availability and hydrophobicity of biochars derived from manure, crop residues, and municipal solid waste for their use as soil amendments. Chemosphere, 2016, 144: 122-130,

Funding

National Natural Science Foundation of China(31972511)