Organic fertilizer substitution alleviates microbial resource limitations to enhance soil function and crop yields

Abstract

Organic-mineral fertilizer combination is a core sustainable agricultural strategy, but its regulatory mechanisms on soil quality and ecosystem multifunctionality (EMF) remain unclear. This study examined 20% nitrogen reduction (RF) and 20% mineral fertilizer substitution with chicken (FF) or cow manure (MF) in north China plain croplands (2022−2023). Compared to conventional fertilization (CF), RF maintained baseline levels of most soilbiochemical characteristics; however, it reduced C-acquisition enzyme activity and EMF in the topsoil (0−20 cm). In contrast, FF and MF increased the soil quality index (SQI, 19%−26%) and EMF (43%−62%) in the topsoil, with positive effects extending to the subsoil (20−40 cm). This was driven by the stimulation of C-, N-, and P-acquisition enzyme activities, alleviated microbial phosphorus limitation, enhanced bacterial diversity, and improved wheat yield by up to 15% relative to CF (p < 0.05). Partial least squares path modeling revealed that soil enzyme activities had a direct, positive effect on both EMF and yield. Soil properties had a direct positive effect on yield (p < 0.001) and directly and indirectly affected EMF by influencing enzyme activities (p < 0.001). This study demonstrates organic substitution enhances soil quality, bacterial diversity, boosts EMF, and increases wheat yield, providing an effective approach for sustainable agriculture production.

Graphical abstract

Keywords

organic fertilizer / microbial metabolic limitation / soil enzyme activity / soil quality index / soil ecosystem multifunctionality

Highlight

	● Combining organic and mineral fertilizer improves both SQI and EMF.
	● C, N, and P nutrient availabilities and microbial biomass are key EMF drivers.
	● Organic fertilizer effectively alleviates the limitation of microbial P in soil.
	● Wheat yield increases with the SQI.

References

[1] Ai, C., Liang, G.Q., Sun, J.W., Wang, X.B., Zhou, W., 2012. Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma173–174, 330–338.

[2] Ai, F., He, L.W., Li, Q., Li, B.B., Zhang, K.Y., Yang, H., Zhang, C.C., 2023. Vermicompost combined with soil conditioner improves the ecosystem multifunctionality in saline-alkali land. Water15, 3075.

[3] Bao, S.D., 2000. Soil Agro-Chemical Analysis. 3rd ed. Beijing: China Agriculture Press.

[4] Bei, S.K., Zhang, Y.L., Li, T.T., Christie, P., Li, X.L., Zhang, J.L., 2018. Response of the soil microbial community to different fertilizer inputs in a wheat-maize rotation on a calcareous soil. Agriculture, Ecosystems & Environment260, 58–69.

[5] Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology and Biochemistry17, 837–842.

[6] Cai, S.J., Wang, F.P., Laws, E.A., Liu, Y., Xu, C., Ma, L.Q., Xiao, W.P., Huang, B.Q., 2022. Linkages between bacterial community and extracellular enzyme activities crossing a coastal front. Ecological Indicators145, 109639.

[7] Chaudhary, S., Dheri, G.S., Brar, B.S., 2017. Long-term effects of NPK fertilizers and organic manures on carbon stabilization and management index under rice-wheat cropping system. Soil and Tillage Research166, 59–66.

[8] Chen, Q.Y., Liu, Z.J., Zhou, J.B., Xu, X.P., Zhu, Y.J., 2021. Long-term straw mulching with nitrogen fertilization increases nutrient and microbial determinants of soil quality in a maize–wheat rotation on China’s Loess Plateau. Science of the Total Environment775, 145930.

[9] Cui, X.W., Zhang, Y.Z., Gao, J.S., Peng, F.Y., Gao, P., 2018. Long-term combined application of manure and chemical fertilizer sustained higher nutrient status and rhizospheric bacterial diversity in reddish paddy soil of central South China. Scientific Reports8, 16554.

[10] Cui, Y.X., Fang, L.C., Guo, X.B., Wang, X., Zhang, Y.J., Li, P.F., Zhang, X.C., 2018. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biology and Biochemistry116, 11–21.

[11] Cui, Z.L., Dou, Z.X., Ying, H., Zhang, F.S., 2020. Producing more with less: reducing environmental impacts through an integrated soil-crop system management approach. Frontiers of Agricultural Science and Engineering7, 14–20.

[12] Dai, X.L., Zhou, W., Liu, G.R., Liang, G.Q., He, P., Liu, Z.B., 2019. Soil C/N and pH together as a comprehensive indicator for evaluating the effects of organic substitution management in subtropical paddy fields after application of high-quality amendments. Geoderma337, 1116–1125.

[13] Du, Z.J., Xiao, Y.T., Qi, X.B., Liu, Y.A., Fan, X.Y., Li, Z.Y., 2018. Peanut-shell biochar and biogas slurry improve soil properties in the North china plain: a four-year field study. Scientific Reports8, 13724.

[14] Feng, H.J., Wang, S.Y., Gao, Z.D., Wang, Z.K., Ren, X.Q., Hu, S.W., Pan, H., 2019. Effect of land use on the composition of bacterial and fungal communities in saline–sodic soils. Land Degradation & Development30, 1851–1860.

[15] Gai, X.P., Liu, H.B., Liu, J., Zhai, L.M., Yang, B., Wu, S.X., Ren, T.Z., Lei, Q.L., Wang, H.Y., 2018. Long-term benefits of combining chemical fertilizer and manure applications on crop yields and soil carbon and nitrogen stocks in North China Plain. Agricultural Water Management208, 384–392.

[16] Gamage, A., Gangahagedara, R., Gamage, J., Jayasinghe, N., Kodikara, N., Suraweera, P., Merah, O., 2023. Role of organic farming for achieving sustainability in agriculture. Farming System1, 100005.

[17] García-Ruiz, R., Ochoa, V., Hinojosa, M.B., Carreira, J.A., 2008. Suitability of enzyme activities for the monitoring of soil quality improvement in organic agricultural systems. Soil Biology and Biochemistry40, 2137–2145.

[18] Garland, G., Banerjee, S., Edlinger, A., Miranda Oliveira, E., Herzog, C., Wittwer, R., Philippot, L., Maestre, F.T., Van Der Heijden, M.G.A., 2021. A closer look at the functions behind ecosystem multifunctionality: a review. Journal of Ecology109, 600–613.

[19] He, H., Peng, M.W., Hou, Z.N., Li, J.H., 2024. Organic substitution contrasting direct fertilizer reduction increases wheat productivity, soil quality, microbial diversity and network complexity. Environmental Technology & Innovation36, 103784.

[20] Ji, L.F., Ni, K., Wu, Z.D., Zhang, J.W., Yi, X.Y., Yang, X.D., Ling, N., You, Z.M., Guo, S.W., Ruan, J.Y., 2020. Effect of organic substitution rates on soil quality and fungal community composition in a tea plantation with long-term fertilization. Biology and fertility of soils56, 633–646.

[21] Jia, R., Zhou, J., Chu, J.C., Shahbaz, M., Yang, Y.D., Jones, D.L., Zang, H.D., Razavi, B.S., Zeng, Z.H., 2022. Insights into the associations between soil quality and ecosystem multifunctionality driven by fertilization management: a case study from the North China Plain. Journal of Cleaner Production362, 132265.

[22] Kuzyakov, Y., Gunina, A., Zamanian, K., Tian, J., Luo, Y., Xu, X.L., Yudina, A., Aponte, H., Alharbi, H., Ovsepyan, L., Kurganova, I., Ge, T.D., Guillaume, T., 2020. New approaches for evaluation of soil health, sensitivity and resistance to degradation. Frontiers of Agricultural Science and Engineering7, 282–288.

[23] Li, A., Strokal, M., Bai, Z.H., Kroeze, C., Ma, L., 2019. How to avoid coastal eutrophication - a back-casting study for the North China plain. Science of the Total Environment692, 676–690.

[24] Li, N., Xu, X., Zhu, Z., Guo, L., Ju, C.H., Zhang, Q., Chen, J., Geng, Q.H., Yang, B.L., Wang, G.B., Shen, C.Q., Cao, G.H., 2023a. Long-term N addition leads to microbial C, but not N limitation of poplar plantation soils in eastern China. Forest Ecology and Management542, 121074.

[25] Li, S.L., Cui, Y.X., Xia, Z.Q., Zhang, X.H., Zhu, M.M., Gao, Y., An, S.Y., Yu, W.T., Ma, Q., 2022a. The mechanism of the dose effect of straw on soil respiration: evidence from enzymatic stoichiometry and functional genes. Soil Biology and Biochemistry168, 108636.

[26] Li, X.Y., Li, B., Chen, L., Liang, J.Y., Huang, R., Tang, X.Y., Zhang, X., Wang, C.Q., 2022b. Partial substitution of chemical fertilizer with organic fertilizer over seven years increases yields and restores soil bacterial community diversity in wheat–rice rotation. European Journal of Agronomy133, 126445.

[27] Ling, J., Zhou, J., Wu, G., Zhao, D.Q., Wang, Z.T., Wen, Y., Zhou, S.L., 2024. Deep-injected straw incorporation enhances subsoil quality and wheat productivity. Plant and Soil499, 207–220.

[28] Liu, B.H., Zhang, Y.L., Yi, X.Y., Zheng, H.T., Ni, K., Ma, Q.X., Cai, Y.J., Ma, L.F., Shi, Y.Z., Yang, X.D., Ruan, J.Y., 2025. Partially replacing chemical fertilizer with manure improves soil quality and ecosystem multifunctionality in a tea plantation. Agriculture, Ecosystems & Environment378, 109284.

[29] Liu, J.A., Shu, A.P., Song, W.F., Shi, W.C., Li, M.C., Zhang, W.X., Li, Z.Z., Liu, G.R., Yuan, F.S., Zhang, S.X., Liu, Z.B., Gao, Z., 2021. Long-term organic fertilizer substitution increases rice yield by improving soil properties and regulating soil bacteria. Geoderma404, 115287.

[30] Loeppmann, S., Blagodatskaya, E., Pausch, J., Kuzyakov, Y., 2016. Enzyme properties down the soil profile - A matter of substrate quality in rhizosphere and detritusphere. Soil Biology and Biochemistry103, 274–283.

[31] Lu, W.D., Hao, Z.Q., Ma, X.L., Gao, J.L., Fan, X.Q., Guo, J.F., Li, J.Q., Lin, M., Zhou, Y.H., 2024. Effects of different proportions of organic fertilizer replacing chemical fertilizer on soil nutrients and fertilizer utilization in gray desert soil. Agronomy14, 228.

[32] Luo, G.W., Rensing, C., Chen, H., Liu, M.Q., Wang, M., Guo, S.W., Ling, N., Shen, Q.R., 2018. Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Functional Ecology32, 1103–1116.

[33] Ma, H.Y., Zhou, J., Ge, J.Y., Nie, J.W., Zhao, J., Xue, Z.Q., Hu, Y.G., Yang, Y.D., Peixoto, L., Zang, H.D., Zeng, Z.H., 2022. Intercropping improves soil ecosystem multifunctionality through enhanced available nutrients but depends on regional factors. Plant and Soil480, 71–84.

[34] Ma, J.F., Chen, Y.P., Wang, K.B., Huang, Y.Z., Wang, H.J., 2021a. Re-utilization of Chinese medicinal herbal residues improved soil fertility and maintained maize yield under chemical fertilizer reduction. Chemosphere283, 131262.

[35] Ma, Z.Z., Zhang, X.C., Zheng, B.Y., Yue, S.C., Zhang, X.C., Zhai, B.N., Wang, Z.H., Zheng, W., Li, Z.Y., Zamanian, K., Razavi, B.S., 2021b. Effects of plastic and straw mulching on soil microbial P limitations in maize fields: dependency on soil organic carbon demonstrated by ecoenzymatic stoichiometry. Geoderma388, 114928.

[36] Moorhead, D.L., Sinsabaugh, R.L., Hill, B.H., Weintraub, M.N., 2016. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology and Biochemistry93, 1–7.

[37] Nath, C.P., Kumar, N., Das, K., Hazra, K.K., Praharaj, C.S., Singh, N.P., 2021. Impact of variable tillage based residue management and legume based cropping for seven years on enzymes activity, soil quality index and crop productivity in rice ecology. Environmental and Sustainability Indicators10, 100107.

[38] Nguyen, B.T., Le, L.B., Pham, L.P., Nguyen, H.T., Tran, T.D., Van Thai, N., 2021. The effects of biochar on the biomass yield of elephant grass (Pennisetum purpureum Schumach) and properties of acidic soils. Industrial Crops and Products161, 113224.

[39] Palaniveloo, K., Amran, M.A., Norhashim, N.A., Mohamad-Fauzi, N., Fang, P.H., Low, H.W., Yap, K.L., Jiale, L., Chian-Yee, M.G., Lai, J.Y., Gunasekaran, B., Razak, S.A., 2020. Food waste composting and microbial community structure profiling. Processes8, 723.

[40] Pokharel, P., Ma, Z.L., Chang, S.X., 2020. Biochar increases soil microbial biomass with changes in extra- and intracellular enzyme activities: a global meta-analysis. Biochar2, 65–79.

[41] Qaswar, M., Jing, H., Ahmed, W., Li, D.C., Liu, S.J., Lu, Z., Cai, A.D., Liu, L.S., Xu, Y.M., Gao, J.S., Zhang, H.M., 2020. Yield sustainability, soil organic carbon sequestration and nutrients balance under long-term combined application of manure and inorganic fertilizers in acidic paddy soil. Soil and Tillage Research198, 104569.

[42] Raza, S., Zamanian, K., Ullah, S., Kuzyakov, Y., Virto, I., Zhou, J.B., 2021. Inorganic carbon losses by soil acidification jeopardize global efforts on carbon sequestration and climate change mitigation. Journal of Cleaner Production315, 128036.

[43] Shakoor, A., Shakoor, S., Rehman, A., Ashraf, F., Abdullah, M., Shahzad, S.M., Farooq, T.H., Ashraf, M., Manzoor, M.A., Altaf, M.M., Altaf, M.A., 2021. Effect of animal manure, crop type, climate zone, and soil attributes on greenhouse gas emissions from agricultural soils—a global meta-analysis. Journal of Cleaner Production278, 124019.

[44] Sheoran, H.S., Kakar, R., Kumar, N., Seema, 2019. Impact of organic and conventional farming practices on soil quality: a global review. Applied Ecology and Environmental Research17, 951–968.

[45] Siedt, M., Schäffer, A., Smith, K.E.C., Nabel, M., Roß-Nickoll, M., Van Dongen, J.T., 2021. Comparing straw, compost, and biochar regarding their suitability as agricultural soil amendments to affect soil structure, nutrient leaching, microbial communities, and the fate of pesticides. Science of the Total Environment751, 141607.

[46] Sünnemann, M., Beugnon, R., Breitkreuz, C., Buscot, F., Cesarz, S., Jones, A., Lehmann, A., Lochner, A., Orgiazzi, A., Reitz, T., Rillig, M.C., Schädler, M., Smith, L.C., Zeuner, A., Guerra, C.A., Eisenhauer, N., 2023. Climate change and cropland management compromise soil integrity and multifunctionality. Communications Earth & Environment4, 394.

[47] Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry19, 703–707.

[48] Wang, C.L., Ma, Y.Q., He, W.H., Kuzyakov, Y., Bol, R., Chen, H.Q., Fan, M.S., 2024. Soil quality and ecosystem multifunctionality after 13-year of organic and nitrogen fertilization. Science of the Total Environment931, 172789.

[49] Wang, L.L., Li, Q., Coulter, J.A., Xie, J.H., Luo, Z.Z., Zhang, R.Z., Deng, X.P., Li, L.L., 2020. Winter wheat yield and water use efficiency response to organic fertilization in Northern China: a meta-analysis. Agricultural Water Management229, 105934.

[50] Wang, Y.F., Chen, P., Wang, F.H., Han, W.X., Qiao, M., Dong, W.X., Hu, C.S., Zhu, D., Chu, H.Y., Zhu, Y.G., 2022. The ecological clusters of soil organisms drive the ecosystem multifunctionality under long-term fertilization. Environment International161, 107133.

[51] Wu, J., Joergensen, R.G., Pommerening, B., Chaussod, R., Brookes, P.C., 1990. Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biology and Biochemistry22, 1167–1169.

[52] Wu, Z.M., Chen, X., Lu, X.C., Zhu, Y.C., Han, X.Z., Yan, J., Yan, L., Zou, W.X., 2024. Impact of combined organic amendments and chemical fertilizers on soil microbial limitations, soil quality, and soybean yield. Plant and Soil507, 317–334.

[53] Xiang, Y.Z., Deng, Q., Duan, H.L., Guo, Y., 2017. Effects of biochar application on root traits: a meta-analysis. GCB Bioenergy9, 1563–1572.

[54] Xiao, L., Liu, G.B., Li, P., Xue, S., 2021. Dynamics of soil specific enzyme activities and temperature sensitivities during grassland succession after farmland abandonment. CATENA199, 105081.

[55] Yang, R.Z., Yang, Z., Yang, S.L., Chen, L.L., Xin, J., Xu, L.Y., Zhang, X.C., Zhai, B.N., Wang, Z.H., Zheng, W., Li, Z.Y., 2023. Nitrogen inhibitors improve soil ecosystem multifunctionality by enhancing soil quality and alleviating microbial nitrogen limitation. Science of the Total Environment880, 163238.

[56] Yuan, M.M., Guo, X., Wu, L.W., Zhang, Y., Xiao, N.J., Ning, D.L., Shi, Z., Zhou, X.S., Wu, L.Y., Yang, Y.F., Tiedje, J.M., Zhou, J.Z., 2021. Climate warming enhances microbial network complexity and stability. Nature Climate Change11, 343–348.

[57] Zeraatpisheh, M., Bakhshandeh, E., Hosseini, M., Alavi, S.M., 2020. Assessing the effects of deforestation and intensive agriculture on the soil quality through digital soil mapping. Geoderma363, 114139.

[58] Zhang, F.S., Cui, Z.L., Fan, M.S., Zhang, W.F., Chen, X.P., Jiang, R.F., 2011. Integrated soil-crop system management: reducing environmental risk while increasing crop productivity and improving nutrient use efficiency in China. Journal of Environmental Quality40, 1051–1057.

[59] Zhang, J.J., Zhu, S.G., Zhu, L.N., Liu, H.T., Yang, J.K., Hua, D.L., 2020. Effects of different amendments on fractions and uptake by winter wheat in slightly alkaline soil contaminated by cadmium and nickel. Environmental Science41, 460–468.

[60] Zhang, W., Xu, Y.D., Gao, D.X., Wang, X., Liu, W.C., Deng, J., Han, X.H., Yang, G.H., Feng, Y.Z., Ren, G.X., 2019. Ecoenzymatic stoichiometry and nutrient dynamics along a revegetation chronosequence in the soils of abandoned land and Robinia pseudoacacia plantation on the Loess Plateau, China. Soil Biology and Biochemistry134, 1–14.

[61] Zhang, X., Davidson, E.A., Mauzerall, D.L., Searchinger, T.D., Dumas, P., Shen, Y., 2015b. Managing nitrogen for sustainable development. Nature528, 51–59.

[62] Zhang, X.Y., Dong, W.Y., Dai, X.Q., Schaeffer, S., Yang, F.T., Radosevich, M., Xu, L.L., Liu, X.Y., Sun, X.M., 2015a. Responses of absolute and specific soil enzyme activities to long term additions of organic and mineral fertilizer. Science of the Total Environment536, 59–67.

[63] Zhao, D.D., Shen, J.Y., Lang, K., Liu, Q.R., Li, Q.Q., 2013. Effects of irrigation and wide-precision planting on water use, radiation interception, and grain yield of winter wheat in the North China Plain. Agricultural Water Management118, 87–92.

[64] Zheng, X.Q., Wei, L., Lv, W.G., Zhang, H.Q., Zhang, Y., Zhang, H.Y., Zhang, H.L., Zhu, Z.K., Ge, T.D., Zhang, W.J., 2024. Long-term bioorganic and organic fertilization improved soil quality and multifunctionality under continuous cropping in watermelon. Agriculture, Ecosystems & Environment359, 108721.

[65] Zhou, F., Zhang, X.C., Ma, S.C., Li, Y., Zhu, M.T., Zhang, W., Li, J., Liu, X., Hu, G.Q., Wang, X.X., He, H.B., Zhang, X.D., 2023. Soil microbial necromass regulation of long-term fertilizer N retention influenced by maize stover mulching. Geoderma433, 116453.

[66] Zhou, L.H., Liu, S.S., Shen, H.H., Zhao, M.Y., Xu, L.C., Xing, A.J., Fang, J.Y., 2020a. Soil extracellular enzyme activity and stoichiometry in China’s forests. Functional Ecology34, 1461–1471.

[67] Zhou, Y., Ma, H.B., Xie, Y.Z., Jia, X.Y., Su, T.T., Li, J.P., Shen, Y., 2020b. Assessment of soil quality indexes for different land use types in typical steppe in the loess hilly area, China. Ecological Indicators118, 106743.

RIGHTS & PERMISSIONS

Higher Education Press