Contrasting effects of biochar and N fertilization on soil heterotrophic and autotrophic respiration in a maize cropland

Abstract

Biochar and nitrogen (N) fertilizer are widely used to improve crop growth and rebuild soil organic carbon (SOC). However, N fertilizer and biochar addition affect SOC unpredictably because of varying effects on soil autotrophic (Ra) and heterotrophic respiration (Rh). To clarify the influence, a field experiment was conducted in which biochar was input alone at rates of 0, 3, 6, and 12 t ha⁻¹ (BC0, BC3, BC6, and BC12) and in combination with urea at 200 kg N ha⁻¹ (BC0U, BC3U, BC6U, and BC12U). Biochar alone had a negligible effect upon Ra regardless of its rate, whereas individual N fertilization promoted Ra by 62.6% than BC0. Conversely, combined N and biochar decreased Ra by 25.9%‒48.2% relative to BC0U, suggesting that biochar and N antagonistically affect Ra. In contrast to Ra, Rh was unresponsive to N alone but showed a significant elevation under biochar at rates of 6 and 12 t ha⁻¹. N fertilization, however, stimulated Rh by 12.1%‒17.7% in biochar-amended soils, suggesting that biochar and N addition synergistically affect Rh. Microbial community analyses indicated that the increased Rh under the incorporation of biochar and N fertilizer might be attributed to the stimulation of copiotrophic microbes. The lowest Rh/SOC ratio was found in BC3U, suggesting a relatively low decomposition rate of SOC. This study highlights that Rs components exhibit distinct responses to individual N fertilization, biochar amendment and their interaction, and suggests that incorporating biochar at the rate of 3 t ha⁻¹ in N-fertilized soil may potentially enhance soil carbon sequestration.

Graphical abstract

Keywords

biochar / autotrophic respiration / heterotrophic respiration / nitrogen availability / interactive effect / soil organic carbon

Highlight

	● Individual addition of fertilizer N and biochar at 6 t ha−1 increased soil autotrophic and heterotrophic respiration, respectively.
	● Biochar counteracted the promotional effect of N ferti-lizer on soil autotrophic respiration.
	● N fertilization accelerated heterotrophic respiration in soils amended with biochar.
	● Combined fertilizer N and biochar raised r/K microbial strategy ratio by supplying nutrients.
	● Combined addition of fertilizer N and biochar at 3 t ha−1 more effectively enhanced soil organic carbon accumulation.

References

[1] Amendola, C., Montagnoli, A., Terzaghi, M., Trupiano, D., Oliva, F., Baronti, S., Miglietta, F., Chiatante, D., Scippa, G.S., 2017. Short-term effects of biochar on grapevine fine root dynamics and arbuscular mycorrhizae production. Agriculture, Ecosystems & Environment239, 236–245.

[2] Bond-Lamberty, B., Thomson, A., 2010. Temperature-associated increases in the global soil respiration record. Nature464, 579–582.

[3] Bowden, R.D., Davidson, E., Savage, K., Arabia, C., Steudler, P., 2004. Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. Forest Ecology and Management196, 43–56.

[4] Che, R.X., Wang, Y.F., Li, K.X., Xu, Z.H., Hu, J.M., Wang, F., Rui, Y.C., Li, L.F., Pang, Z., Cui, X.Y., 2019. Degraded patch formation significantly changed microbial community composition in alpine meadow soils. Soil and Tillage Research195, 104426.

[5] Chen, G.H., Fang, Y.Y., Van Zwieten, L., Xuan, Y.X., Tavakkoli, E., Wang, X.J., Zhang, R.D., 2021. Priming, stabilization and temperature sensitivity of native SOC is controlled by microbial responses and physicochemical properties of biochar. Soil Biology and Biochemistry154, 108139.

[6] Chen, G.S., Yang, Y.S., Robinson, D., 2013. Allocation of gross primary production in forest ecosystems: allometric constraints and environmental responses. New Phytologist200, 1176–1186.

[7] Chen, Z.M., Xu, Y.H., Castellano, M.J., Fontaine, S., Wang, W.J., Ding, W.X., 2019. Soil respiration components and their temperature sensitivity under chemical fertilizer and compost application: the role of nitrogen supply and compost substrate quality. Journal of Geophysical Research: Biogeosciences124, 556–571.

[8] Chen, Z.M., Xu, Y.H., Fan, J.L., Yu, H.Y., Ding, W.X., 2017. Soil autotrophic and heterotrophic respiration in response to different N fertilization and environmental conditions from a cropland in Northeast China. Soil Biology and Biochemistry110, 103–115.

[9] Chen, Z.M., Xu, Y.H., He, Y.J., Zhou, X.H., Fan, J.L., Yu, H.Y., Ding, W.X., 2018. Nitrogen fertilization stimulated soil heterotrophic but not autotrophic respiration in cropland soils: a greater role of organic over inorganic fertilizer. Soil Biology and Biochemistry116, 253–264.

[10] Cheng, H.G., Hill, P.W., Bastami, M.S., Jones, D.L., 2017. Biochar stimulates the decomposition of simple organic matter and suppresses the decomposition of complex organic matter in a sandy loam soil. GCB Bioenergy9, 1110–1121.

[11] Chinese Soil Society, 2000. Analytical Methods of Soil Agrochemistry. Beijing: China Agricultural Science and Technology Press.

[12] Creamer, C.A., de Menezes, A.B., Krull, E.S., Sanderman, J., Newton-Walters, R., Farrell, M., 2015. Microbial community structure mediates response of soil C decomposition to litter addition and warming. Soil Biology and Biochemistry80, 175–188.

[13] Cusack, D.F., Torn, M.S., McDowell, W.H., Silver, W.L., 2010. The response of heterotrophic activity and carbon cycling to nitrogen additions and warming in two tropical soils. Global Change Biology16, 2555–2572.

[14] Ding, W.X., Meng, L., Yin, Y.F., Cai, Z.C., Zheng, X.H., 2007. CO₂ emission in an intensively cultivated loam as affected by long-term application of organic manure and nitrogen fertilizer. Soil Biology and Biochemistry39, 669–679.

[15] Ding, W.X., Yu, H.Y., Cai, Z.C., Han, F.X., Xu, Z.H., 2010. Responses of soil respiration to N fertilization in a loamy soil under maize cultivation. Geoderma155, 381–389.

[16] Edgar, R.C., 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods10, 996–998.

[17] Elzobair, K.A., Stromberger, M.E., Ippolito, J.A., 2016. Stabilizing effect of biochar on soil extracellular enzymes after a denaturing stress. Chemosphere142, 114–119.

[18] Fan, J.L., Ding, W.X., Xiang, J., Qin, S.W., Zhang, J.B., Ziadi, N., 2014. Carbon sequestration in an intensively cultivated sandy loam soil in the North China Plain as affected by compost and inorganic fertilizer application. Geoderma230−231, 22–28.

[19] Farrell, M., Kuhn, T.K., Macdonald, L.M., Maddern, T.M., Murphy, D.V., Hall, P.A., Singh, B.P., Baumann, K., Krull, E.S., Baldock, J.A., 2013. Microbial utilisation of biochar-derived carbon. Science of the Total Environment465, 288–297.

[20] Fierer, N., Bradford, M.A., Jackson, R.B., 2007. Toward an ecological classification of soil bacteria. Ecology88, 1354–1364.

[21] Fu, Y.Y., Luo, Y., Auwal, M., Singh, B.P., Van Zwieten, L., Xu, J.M., 2022. Biochar accelerates soil organic carbon mineralization via rhizodeposit-activated Actinobacteria. Biology and Fertility of Soils58, 565–577.

[22] Gul, S., Whalen, J.K., 2016. Biochemical cycling of nitrogen and phosphorus in biochar-amended soils. Soil Biology and Biochemistry103, 1–15.

[23] Haider, G., Steffens, D., Müller, C., Kammann, C.I., 2016. Standard extraction methods may underestimate nitrate stocks captured by field-aged biochar. Journal of Environmental Quality45, 1196–1204.

[24] Han, J.L., Zhang, A.F., Kang, Y.H., Han, J.Q., Yang, B., Hussain, Q., Wang, X.D., Zhang, M., Khan, M.A., 2022. Biochar promotes soil organic carbon sequestration and reduces net global warming potential in apple orchard: a two-year study in the Loess Plateau of China. Science of the Total Environment803, 150035.

[25] Hoe, S.L., 2008. Issues and procedures in adopting structural equation modelling technique. Journal of Quantitative Methods3, 76–83.

[26] Huang, G., Li, L., Su, Y.G., Li, Y., 2018. Differential seasonal effects of water addition and nitrogen fertilization on microbial biomass and diversity in a temperate desert. CATENA161, 27–36.

[27] Janssens, I.A., Dieleman, W., Luyssaert, S., Subke, J.A., Reichstein, M., Ceulemans, R., Ciais, P., Dolman, A.J., Grace, J., Matteucci, G., Papale, D., Piao, S.L., Schulze, E.D., Tang, J., Law, B.E., 2010. Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience3, 315–322.

[28] Joseph, S., Cowie, A.L., Van Zwieten, L., Bolan, N., Budai, A., Buss, W., Cayuela, M.L., Graber, E.R., Ippolito, J.A., Kuzyakov, Y., Luo, Y., Ok, Y.S., Palansooriya, K.N., Shepherd, J., Stephens, S., Weng, Z., Lehmann, J., 2021. How biochar works, and when it doesn't: a review of mechanisms controlling soil and plant responses to biochar. GCB Bioenergy13, 1731–1764.

[29] Kuzyakov, Y., Bogomolova, I., Glaser, B., 2014. Biochar stability in soil: decomposition during eight years and transformation as assessed by compound-specific ¹⁴C analysis. Soil Biology and Biochemistry70, 229–236.

[30] Lal, R., 2018. Digging deeper: a holistic perspective of factors affecting soil organic carbon sequestration in agroecosystems. Global Change Biology24, 3285–3301.

[31] Lei, J.S., Guo, X., Zeng, Y.F., Zhou, J.Z., Gao, Q., Yang, Y.F., 2021. Temporal changes in global soil respiration since 1987. Nature Communications12, 403.

[32] Li, H., Yang, S., Semenov, M.V., Yao, F., Ye, J., Bu, R.C. Ma, R.A., Lin, J.J., Kurganova, I., Wang, X.G., Deng, Y., Kravchenko, I., Jiang, Y., Kuzyakov, Y., 2021. Temperature sensitivity of SOM decomposition is linked with a K-selected microbial community. Global Change Biology27, 2763–2779.

[33] Li, S.L., Liang, C.T., Shangguan, Z.P., 2017. Effects of apple branch biochar on soil C mineralization and nutrient cycling under two levels of N. Science of the Total Environment607−608, 109–119.

[34] Li, S.L., Wang, S., Fan, M.C., Wu, Y., Shangguan, Z.P., 2020. Interactions between biochar and nitrogen impact soil carbon mineralization and the microbial community. Soil and Tillage Research196, 104437.

[35] Li, W.B., Jin, C.J., Guan, D.X., Wang, Q.K., Wang, A.Z., Yuan, F.H., Wu, J.B., 2015. The effects of simulated nitrogen deposition on plant root traits: a meta-analysis. Soil Biology and Biochemistry82, 112–118.

[36] Li, Y.F., Zhang, S.B., Fang, Y.Y., Hui, D.F., Tang, C.X., Van Zwieten, L., Zhou, J.S., Jiang, Z.H., Cai, Y.J., Yu, B., Hu, J.G., Zhou, G.M., Gu, B.J., Chang, S.X., 2024. Nitrogen deposition-induced stimulation of soil heterotrophic respiration is counteracted by biochar in a subtropical forest. Agricultural and Forest Meteorology349, 109940.

[37] Liao, X., Müller, C., Jansen-Willems, A., Luo, J.F., Lindsey, S., Liu, D.Y., Chen, Z.M., Niu, Y.H., Ding, W.X., 2021. Field-aged biochar decreased N₂O emissions by reducing autotrophic nitrification in a sandy loam soil. Biology and Fertility of Soils57, 471–483.

[38] Ling, J., Dungait, J.A.J., Delgado-Baquerizo, M., Cui, Z.L., Zhou, R.R., Zhang, W.S., Gao, Q., Chen, Y.X., Yue, S.C., Kuzyakov, Y., Zhang, F.S., Chen, X.P., Tian, J., 2025. Soil organic carbon thresholds control fertilizer effects on carbon accrual in croplands worldwide. Nature Communications16, 3009.

[39] Liu, Q., Liu, B.J., Zhang, Y.H., Hu, T.L., Lin, Z.B., Liu, G., Wang, X.J., Ma, J.; Wang, H., Jin, H.Y., Ambus, P., Amonette, J.E., Xie, Z.B., 2019. Biochar application as a tool to decrease soil nitrogen losses (NH₃ volatilization, N₂O emissions, and N leaching) from croplands: options and mitigation strength in a global perspective. Global Change Biology25, 2077–2093.

[40] Louca, S., Parfrey, L.W., Doebeli, M., 2016. Decoupling function and taxonomy in the global ocean microbiome. Science353, 1272–1277.

[41] Lu, W.W., Ding, W.X., Zhang, J.H., Li, Y., Luo, J.F., Bolan, N., Xie, Z.B., 2014. Biochar suppressed the decomposition of organic carbon in a cultivated sandy loam soil: a negative priming effect. Soil Biology and Biochemistry76, 12–21.

[42] Lu, X.H., Li, Y.F., Wang, H.L., Singh, B.P., Hu, S.D., Luo, Y., Li, J.W., Xiao, Y.H., Cai, X.Q., Li, Y.C., 2019. Responses of soil greenhouse gas emissions to different application rates of biochar in a subtropical Chinese chestnut plantation. Agricultural and Forest Meteorology271, 168–179.

[43] Luo, S.S., Wang, S.J., Tian, L., Li, S.Q., Li, X.J., Shen, Y.F., Tian, C.J., 2017. Long-term biochar application influences soil microbial community and its potential roles in semiarid farmland. Applied Soil Ecology117–118, 10–15.

[44] Ma, N.N., Zhang, L.L., Zhang, Y.L., Yang, L.J., Yu, C.X., Yin, G.H., Doane, T.A., Wu, Z.J., Zhu, P., Ma, X.Z., 2016. Biochar improves soil aggregate stability and water availability in a mollisol after three years of field application. PLoS One11, e0154091.

[45] Mogollón, J.M., Lassaletta, L., Beusen, A.H. W., Van Grinsven, H.J. M., Westhoek, H., Bouwman, A.F., 2018. Assessing future reactive nitrogen inputs into global croplands based on the shared socioeconomic pathways. Environmental Research Letters13, 044008.

[46] Mukhamed, B., Tian, L.X., Yu, S.P., Gao, X.L., Feng, B.L., 2024. Biochar amendment has stronger effects than fertilizer regimes on the bacterial community structure and ecological processes in broomcorn millet field on the Loess Plateau. Plant and Soil499, 237–253.

[47] Niu, Y.H., Chen, Z.M., Müller, C., Zaman, M.M., Kim, D., Yu, H.Y., Ding, W.X., 2017. Yield-scaled N₂O emissions were effectively reduced by biochar amendment of sandy loam soil under maize-wheat rotation in the North China Plain. Atmospheric Environment170, 58–70.

[48] Rosenzweig, S.T., Schipanski, M.E., Kaye, J.P., 2017. Rhizosphere priming and plant-mediated cover crop decomposition. Plant and Soil417, 127–139.

[49] Sanderman, J., Hengl, T., Fiske, G.J., 2017. Soil carbon debt of 12, 000 years of human land use. Proceedings of the National Academy of Sciences of the United States of America114, 9575–9580.

[50] Schmidt, H.P., Kammann, C., Hagemann, N., Leifeld, J., Bucheli, T.D., Sánchez Monedero, M.A., Cayuela, M.L., 2021. Biochar in agriculture-A systematic review of 26 global meta-analyses. GCB Bioenergy13, 1708–1730.

[51] Schröder, J.J., Neeteson, J.J., Oenema, O., Struik, P.C., 2000. Does the crop or the soil indicate how to save nitrogen in maize production?: Reviewing the state of the art. Field Crops Research66, 151–164.

[52] Shao, P., Zeng, X.B., Moore, D.J.P., Zeng, X.D., 2013. Soil microbial respiration from observations and Earth system models. Environmental Research Letters8, 034034.

[53] Shi, X.Z., Yang, G.X., Yu, D.S., Xu, S.X., Warner, E.D., Petersen, G.W., Sun, W.X., Zhao, Y.C., Easterling, W.E., Wang, H.J., 2010. A WebGIS system for relating genetic soil classification of China to soil taxonomy. Computers & Geosciences36, 768–775.

[54] Singh, B.P., Cowie, A.L., 2014. Long-term influence of biochar on native organic carbon mineralisation in a low-carbon clayey soil. Scientific Reports4, 3687.

[55] Sokol, N.W., Sanderman, J., Bradford, M.A., 2019. Pathways of mineral-associated soil organic matter formation: integrating the role of plant carbon source, chemistry, and point of entry. Global Change Biology25, 12–24.

[56] Tu, L.H., Hu, T.X., Zhang, J., Li, X.W., Hu, H.L., Liu, L., Xiao, Y.L., 2013. Nitrogen addition stimulates different components of soil respiration in a subtropical bamboo ecosystem. Soil Biology and Biochemistry58, 255–264.

[57]

[58] Ventura, M., Zhang, C., Baldi, E., Fornasier, F., Sorrenti, G., Panzacchi, P., Tonon, G., 2014. Effect of biochar addition on soil respiration partitioning and root dynamics in an apple orchard. European Journal of Soil Science65, 186–195.

[59] Wang, R.Z., Bicharanloo, B., Shirvan, M.B., Cavagnaro, T.R., Jiang, Y., Keitel, C., Dijkstra, F.A., 2021. A novel ¹³C pulse-labelling method to quantify the contribution of rhizodeposits to soil respiration in a grassland exposed to drought and nitrogen addition. New Phytologist230, 857–866.

[60] Whitman, T., Enders, A., Lehmann, J., 2014. Pyrogenic carbon additions to soil counteract positive priming of soil carbon mineralization by plants. Soil Biology and Biochemistry73, 33–41.

[61] Wiesmeier, M., Hübner, R., Kögel-Knabner, I., 2015. Stagnating crop yields: an overlooked risk for the carbon balance of agricultural soils?. Science of the Total Environment536, 1045–1051.

[62] Wu, L., Zhang, W.J., Wei, W.J., He, Z.L., Kuzyakov, Y., Bol, R., Hu, R.G., 2019. Soil organic matter priming and carbon balance after straw addition is regulated by long-term fertilization. Soil Biology and Biochemistry135, 383–391.

[63] Xing, W., Lu, X.M., Ying, J.Y., Lan, Z.C., Chen, D.M., Bai, Y.F., 2022. Disentangling the effects of nitrogen availability and soil acidification on microbial taxa and soil carbon dynamics in natural grasslands. Soil Biology and Biochemistry164, 108495.

[64] Xu, S.Y., Chen, J.F., Peng, H.Y., Leng, S.Q., Li, H., Qu, W.Q., Hu, Y.C., Li, H.L., Jiang, S.J., Zhou, W.G., Leng, L.J., 2021. Effect of biomass type and pyrolysis temperature on nitrogen in biochar, and the comparison with hydrochar. Fuel291, 120128.

[65] Xu, Y.H., Chen, Z.M., Fontaine, S., Wang, W.J., Luo, J.F., Fan, J.L., Ding, W.X., 2017. Dominant effects of organic carbon chemistry on decomposition dynamics of crop residues in a Mollisol. Soil Biology and Biochemistry115, 221–232.

[66] Yan, W.M., Zhong, Y.Q. W., Liu, J., Shangguan, Z.P., 2021. Response of soil respiration to nitrogen fertilization: evidence from a 6-year field study of croplands. Geoderma384, 114829.

[67] Yang, X., Meng, J., Lan, Y., Chen, W.F., Yang, T.X., Yuan, J., Liu, S.N., Han, J., 2017. Effects of maize stover and its biochar on soil CO₂ emissions and labile organic carbon fractions in Northeast China. Agriculture, Ecosystems & Environment240, 24–31.

[68] Yang, Y., Li, T., Pokharel, P., Liu, L.X., Qiao, J.B., Wang, Y.Q., An, S.S., Chang, S.X., 2022. Global effects on soil respiration and its temperature sensitivity depend on nitrogen addition rate. Soil Biology and Biochemistry174, 108814.

[69] Ye, L.L., Camps-Arbestain, M., Shen, Q.H., Lehmann, J., Singh, B., Sabir, M., 2020. Biochar effects on crop yields with and without fertilizer: a meta-analysis of field studies using separate controls. Soil Use and Management36, 2–18.

[70] Zak, D.R., Pregitzer, K.S., Curtis, P.S., Teeri, J.A., Fogel, R., Randlett, D.L., 1993. Elevated atmospheric CO₂ and feedback between carbon and nitrogen cycles. Plant and Soil151, 105–117.

[71] Zebarth, B.J., Rochette, P., Burton, D.L., 2008. N₂O emissions from spring barley production as influenced by fertilizer nitrogen rate. Canadian Journal of Soil Science88, 197–205.

[72] Zhang, C., Song, Z.L., Zhuang, D.H., Wang, J., Xie, S.S., Liu, G.B., 2019. Urea fertilization decreases soil bacterial diversity, but improves microbial biomass, respiration, and N-cycling potential in a semiarid grassland. Biology and Fertility of Soils55, 229–242.

[73] Zhang, J.J., Li, Y., Wang, J.S., Chen, W.N., Tian, D.S., Niu, S.L., 2021a. Different responses of soil respiration and its components to nitrogen and phosphorus addition in a subtropical secondary forest. Forest Ecosystems8, 37.

[74] Zhang, S.B., Li, Y.F., Singh, B.P., Wang, H.L., Cai, X.Q., Chen, J.H., Qin, H., Li, Y.C., Chang, S.X., 2021b. Contrasting short-term responses of soil heterotrophic and autotrophic respiration to biochar-based and chemical fertilizers in a subtropical Moso bamboo plantation. Applied Soil Ecology157, 103758.

[75] Zhao, X., Yan, X.Y., Wang, S.Q., Xing, G.X., Zhou, Y., 2013. Effects of the addition of rice-straw-based biochar on leaching and retention of fertilizer N in highly fertilized cropland soils. Soil Science and Plant Nutrition59, 771–782.

[76] Zhou, J.S., Zhang, S.B., Hui, D.F., Vancov, T., Fang, Y.Y., Tang, C.X., Jiang, Z.H., Ge, T.D., Cai, Y.J., Yu, B., White, J.C., Li, Y.F., 2024. Pyrogenic organic matter decreases while fresh organic matter increases soil heterotrophic respiration through modifying microbial activity in a subtropical forest. Biology and Fertility of Soils60, 509–524.

RIGHTS & PERMISSIONS

Higher Education Press