Long-term organic fertilization fosters modular microbial networks: A global analysis of soil bacteriome responses

Abstract

Fertilization is a widely adopted agricultural practice with profound impacts on soil microbial communities. However, the global response of soil bacteriome to different fertilization strategies remains inadequately characterized. Here, we conducted an integrated analysis on over 2900 raw bacterial amplicon sequencing samples from 82 studies worldwide to assess how microbial communities respond to inorganic (IF), organic (OF), and combined (IFOF) fertilization across environmental gradients. Results demonstrate that the effects of fertilization on community structure and diversity depend strongly on local soil properties, although OF maintained stable alpha-diversity across varying pH and experimental durations. Notably, meta-cooccurrence networks revealed that organic amendments (OF and IFOF) promoted microbial networks with higher complexity, modularity, and stability compared to IF and unfertilized controls, suggesting strengthened ecological resilience. The IFOF network contained several highly connected keystone taxa including Acidothermus, Devosia, and Bradyrhizobium, which exhibited sensitivity to gradients in soil nutrients, pH, and climate variables. Random forest models further confirmed the ecological importance of these taxa, achieving high accuracy (>90%) in classifying fertilization treatments. Moreover, threshold indicator taxon analysis quantified responses of these keystone taxa to environmental gradients, identifying optimal organic fertilization amendment rates to support keystone taxa (e.g., Bradyrhizobium abundance peaked at 15 tons per hectare per year). This study provides the first global-scale integration of sequencing data with meta-network analysis, revealing how long-term fertilization influences soil microbial communities and associations.

Graphical abstract

Keywords

long-term fertilization / soil / bacteriome / network analysis / keystone taxa

Highlight

	● Over 2900 amplicon sequencing samples worldwide were integrated and analyzed.
	● Global meta-network analysis reveals fertilization-induced ecological patterns.
	● Organic fertilization generally enhances microbial network modularity and stability.
	● Keystone taxa exhibit quantitative thresholds to environmental gradients.

References

[1] Asaf, S., Numan, M., Khan, A.L., Al-Harrasi, A., 2020. Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Critical Reviews in Biotechnology40, 138–152.

[2] Baker, M.E., King, R.S., 2010. A new method for detecting and interpreting biodiversity and ecological community thresholds. Methods in Ecology and Evolution1, 25–37.

[3] Banerjee, S., Schlaeppi, K., van der Heijden, M.G.A., 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology16, 567–576.

[4] Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: An open source software for exploring and manipulating networks. In: Proceedings of the International AAAI Conference on Web and Social Media. AAAI361–362.

[5] Becraft, E.D., Woyke, T., Jarett, J., Ivanova, N., Godoy-Vitorino, F., Poulton, N., Brown, J.M., Brown, J., Lau, M.C.Y., Onstott, T., Eisen, J.A., Moser, D., Stepanauskas, R., 2017. Rokubacteria: genomic giants among the uncultured bacterial phyla. Frontiers in Microbiology8, 2264.

[6] Bender, S.F., Wagg, C., van der Heijden, M.G.A., 2016. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends in Ecology & Evolution31, 440–452.

[7] Benjamini, Y., Krieger, A.M., Yekutieli, D., 2006. Adaptive linear step-up procedures that control the false discovery rate. Biometrika93, 491–507.

[8] Berry, D., Widder, S., 2014. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Frontiers in Microbiology5, 219.

[9] Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al-Ghalith, G.A., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J.E., Bittinger, K., Brejnrod, A., Brislawn, C.J., Brown, C.T., Callahan, B.J., Caraballo-Rodríguez, A.M., Chase, J., Cope, E.K., Da Silva, R., Diener, C., Dorrestein, P.C., Douglas, G.M., Durall, D.M., Duvallet, C., Edwardson, C.F., Ernst, M., Estaki, M., Fouquier, J., Gauglitz, J.M., Gibbons, S.M., Gibson, D.L., Gonzalez, A., Gorlick, K., Guo, J.R., Hillmann, B., Holmes, S., Holste, H., Huttenhower, C., Huttley, G.A., Janssen, S., Jarmusch, A.K., Jiang, L.J., Kaehler, B.D., Kang, K.B., Keefe, C.R., Keim, P., Kelley, S.T., Knights, D., Koester, I., Kosciolek, T., Kreps, J., Langille, M.G.I., Lee, J., Ley, R., Liu, Y.X., Loftfield, E., Lozupone, C., Maher, M., Marotz, C., Martin, B.D., McDonald, D., McIver, L.J., Melnik, A.V., Metcalf, J.L., Morgan, S.C., Morton, J.T., Naimey, A.T., Navas-Molina, J.A., Nothias, L.F., Orchanian, S.B., Pearson, T., Peoples, S.L., Petras, D., Preuss, M.L., Pruesse, E., Rasmussen, L.B., Rivers, A., Robeson, M.S., Rosenthal, P., Segata, N., Shaffer, M., Shiffer, A., Sinha, R., Song, S.J., Spear, J.R., Swafford, A.D., Thompson, L.R., Torres, P.J., Trinh, P., Tripathi, A., Turnbaugh, P.J., Ul-Hasan, S., van der Hooft, J.J.J., Vargas, F., Vázquez-Baeza, Y., Vogtmann, E., von Hippel, M., Walters, W., Wan, Y.H., Wang, M.X., Warren, J., Weber, K.C., Williamson, C.H.D., Willis, A.D., Xu, Z.Z., Zaneveld, J.R., Zhang, Y.L., Zhu, Q.Y., Knight, R., Caporaso, J.G., 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology37, 852–857.

[10] Brewer, T.E., Handley, K.M., Carini, P., Gilbert, J.A., Fierer, N., 2016. Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’. Nature Microbiology2, 16198.

[11] Caporaso, J.G., Lauber, C.L., Walters, W.A., et al., et al. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America108, 4516–4522.

[12] Chen, C., Li, S.L., Chen, Q.L., Delgado-Baquerizo, M., Guo, Z.F., Wang, F.H., Xu, Y.Y., Zhu, Y.G., 2024a. Fertilization regulates global thresholds in soil bacteria. Global Change Biology30, e17466.

[13] Chen, S., Cheng, H.C., Wyckoff, K.N., He, Q., 2016. Linkages of Firmicutes and Bacteroidetes populations to methanogenic process performance. Journal of Industrial Microbiology and Biotechnology43, 771–781.

[14] Chen, Y.N., Li, Y., Qiu, T.Y., He, H.R., Liu, J., Duan, C.J., Cui, Y.X., Huang, M., Wu, C.Y., Fang, L.C., 2024b. High nitrogen fertilizer input enhanced the microbial network complexity in the paddy soil. Soil Ecology Letters6, 230205.

[15] Chhetri, G., Kim, I., Kang, M., Kim, J., So, Y., Seo, T., 2022. Devosia rhizoryzae sp. nov., and Devosia oryziradicis sp. nov., novel plant growth promoting members of the genus Devosia, isolated from the rhizosphere of rice plants. Journal of Microbiology60, 1–10.

[16] Clauset, A., Newman, M.E.J., Moore, C., 2004. Finding community structure in very large networks. Physical Review E70, 066111.

[17] Cui, J.W., Zhu, R.L., Wang, X.Y., Xu, X.P., Ai, C., He, P., Liang, G.Q., Zhou, W., Zhu, P., 2022. Effect of high soil C/N ratio and nitrogen limitation caused by the long-term combined organic-inorganic fertilization on the soil microbial community structure and its dominated SOC decomposition. Journal of Environmental Management303, 114155.

[18] Dai, Z.M., Su, W.Q., Chen, H.H., Barberán, A., Zhao, H.C., Yu, M.J., Yu, L., Brookes, P.C., Schadt, C.W., Chang, S.X., Xu, J.M., 2018. Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro-ecosystems across the globe. Global Change Biology24, 3452–3461.

[19] Dang, P.F., Li, C.F., Lu, C., Zhang, M.M., Huang, T.T., Wan, C.X., Wang, H.Y., Chen, Y.L., Qin, X.L., Liao, Y.C., Siddique, K.H.M., 2022. Effect of fertilizer management on the soil bacterial community in agroecosystems across the globe. Agriculture, Ecosystems & Environment326, 107795.

[20] Delgado-Baquerizo, M., Reich, P.B., Trivedi, C., Eldridge, D.J., Abades, S., Alfaro, F.D., Bastida, F., Berhe, A.A., Cutler, N.A., Gallardo, A., García-Velázquez, L., Hart, S.C., Hayes, P.E., He, J.Z., Hseu, Z.Y., Hu, H.W., Kirchmair, M., Neuhauser, S., Pérez, C.A., Reed, S.C., Santos, F., Sullivan, B.W., Trivedi, P., Wang, J.T., Weber-Grullon, L., Williams, M.A., Singh, B.K., 2020. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution4, 210–220.

[21] Fan, K.K., Delgado-Baquerizo, M., Guo, X.S., Wang, D.Z., Zhu, Y.G., Chu, H.Y., 2021. Biodiversity of key-stone phylotypes determines crop production in a 4-decade fertilization experiment. The ISME Journal15, 550–561.

[22] Feng, Y.Z., Delgado-Baquerizo, M., Zhu, Y.G., Han, X.Z., Han, X.R., Xin, X.L., Li, W., Guo, Z.B., Dang, T.H., Li, C.H., Zhu, B., Cai, Z.J., Li, D.M., Zhang, J.B., 2022. Responses of soil bacterial diversity to fertilization are driven by local environmental context across China. Engineering12, 164–170.

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

[24] Geisseler, D., Linquist, B.A., Lazicki, P.A., 2017. Effect of fertilization on soil microorganisms in paddy rice systems – A meta-analysis. Soil Biology and Biochemistry115, 452–460.

[25] Geisseler, D., Scow, K.M., 2014. Long-term effects of mineral fertilizers on soil microorganisms – A review. Soil Biology and Biochemistry75, 54–63.

[26] Griffiths, B.S., Philippot, L., 2013. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiology Reviews37, 112–129.

[27] Grilli, J., Rogers, T., Allesina, S., 2016. Modularity and stability in ecological communities. Nature Communications7, 12031.

[28] Gui, H., Breed, M., Li, Y., Xu, Q., Yang, J.B., Wanasinghe, D.N., Li, Y.J., Xu, J.C., Mortimer, P., 2023. Continental-scale insights into the soil microbial co-occurrence networks of Australia and their environmental drivers. Soil Biology and Biochemistry186, 109177.

[29] Hartman, K., van der Heijden, M.G.A., Wittwer, R.A., Banerjee, S., Walser, J.C., Schlaeppi, K., 2018. Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming. Microbiome6, 14.

[30] Hartmann, M., Six, J., 2023. Soil structure and microbiome functions in agroecosystems. Nature Reviews Earth & Environment4, 4–18.

[31] Hill, T.C.J., Walsh, K.A., Harris, J.A., Moffett, B.F., 2003. Using ecological diversity measures with bacterial communities. FEMS Microbiology Ecology43, 1–11.

[32] Kim, J.J., Seong, H.J., Johnson, T.A., Cha, C.J., Sul, W.J., Chae, J.C., 2023. Persistence of antibiotic resistance from animal agricultural effluents to surface water revealed by genome-centric metagenomics. Journal of Hazardous Materials457, 131761.

[33] Kruczyńska, A., Kuźniar, A., Podlewski, J., Słomczewski, A., Grządziel, J., Marzec-Grządziel, A., Gałązka, A., Wolińska, A., 2023. Bacteroidota structure in the face of varying agricultural practices as an important indicator of soil quality – a culture independent approach. Agriculture, Ecosystems & Environment342, 108252.

[34] Kuypers, M.M.M., Marchant, H.K., Kartal, B., 2018. The microbial nitrogen-cycling network. Nature Reviews Microbiology16, 263–276.

[35] Laborde, D., Mamun, A., Martin, W., Piñeiro, V., Vos, R., 2021. Agricultural subsidies and global greenhouse gas emissions. Nature Communications12, 2601.

[36] Labouyrie, M., Ballabio, C., Romero, F., Panagos, P., Jones, A., Schmid, M.W., Mikryukov, V., Dulya, O., Tedersoo, L., Bahram, M., Lugato, E., van der Heijden, M.G.A., Orgiazzi, A., 2023. Patterns in soil microbial diversity across Europe. Nature Communications14, 3311.

[37] Lewin, S., Francioli, D., Ulrich, A., Kolb, S., 2021. Crop host signatures reflected by co-association patterns of keystone Bacteria in the rhizosphere microbiota. Environmental Microbiome16, 18.

[38] Li, B.B., Roley, S.S., Duncan, D.S., Guo, J.R., Quensen, J.F., Yu, H.Q., Tiedje, J.M., 2021. Long-term excess nitrogen fertilizer increases sensitivity of soil microbial community to seasonal change revealed by ecological network and metagenome analyses. Soil Biology and Biochemistry160, 108349.

[39] Liaw, A., Wiener, M. 2002. Classification and regression by randomForest. R News2, 18–22.

[40] Lin, Y.X., Ye, G.P., Kuzyakov, Y., Liu, D.Y., Fan, J.B., Ding, W.X., 2019. Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biology and Biochemistry134, 187–196.

[41] Ling, N., Zhu, C., Xue, C., Chen, H., Duan, Y.H., Peng, C., Guo, S.W., Shen, Q.R., 2016. Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biology and Biochemistry99, 137–149.

[42] Liu, T., Wu, X.H., Li, H.W., Alharbi, H., Wang, J., Dang, P., Chen, X.Y., Kuzyakov, Y., Yan, W.D., 2020. Soil organic matter, nitrogen and pH driven change in bacterial community following forest conversion. Forest Ecology and Management477, 118473.

[43] Liu, Z.T., Ma, R.A., Zhu, D., Konstantinidis, K.T., Zhu, Y.G., Zhang, S.Y., 2024. Organic fertilization co-selects genetically linked antibiotic and metal(loid) resistance genes in global soil microbiome. Nature Communications15, 5168.

[44] Luo, F., Zhong, J.X., Yang, Y.F., Scheuermann, R.H., Zhou, J.Z., 2006. Application of random matrix theory to biological networks. Physics Letters A357, 420–423.

[45] Luo, G.W., Li, L., Friman, V.P., Guo, J.J., Guo, S.W., Shen, Q.R., Ling, N., 2018. Organic amendments increase crop yields by improving microbe-mediated soil functioning of agroecosystems: a meta-analysis. Soil Biology and Biochemistry124, 105–115.

[46] Luo, J.P., Liao, G.C., Banerjee, S., Gu, S.H., Liang, J.B., Guo, X.Y., Zhao, H.P., Liang, Y.C., Li, T.Q., 2023. Long-term organic fertilization promotes the resilience of soil multifunctionality driven by bacterial communities. Soil Biology and Biochemistry177, 108922.

[47] Ma, B., Wang, H.Z., Dsouza, M., Lou, J., He, Y., Dai, Z.M., Brookes, P.C., Xu, J.M., Gilbert, J.A., 2016. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. The ISME Journal10, 1891–1901.

[48] Ma, Y.J., Shen, S.Z., Wan, C., Wang, S.Q., Yang, F.X., Zhang, K.Q., Gao, W.X., 2023. Organic fertilizer substitution over six years improves the productivity of garlic, bacterial diversity, and microbial communities network complexity. Applied Soil Ecology182, 104718.

[49] Martre, P., Dueri, S., Guarin, J.R., Ewert, F., Webber, H., Calderini, D., Molero, G., Reynolds, M., Miralles, D., Garcia, G., Brown, H., George, M., Craigie, R., Cohan, J.P., Deswarte, J.C., Slafer, G., Giunta, F., Cammarano, D., Ferrise, R., Gaiser, T., Gao, Y.J., Hochman, Z., Hoogenboom, G., Hunt, L.A., Kersebaum, K.C., Nendel, C., Padovan, G., Ruane, A.C., Srivastava, A.K., Stella, T., Supit, I., Thorburn, P., Wang, E.L., Wolf, J., Zhao, C., Zhao, Z.G., Asseng, S., 2024. Global needs for nitrogen fertilizer to improve wheat yield under climate change. Nature Plants10, 1081–1090.

[50] Olesen, J.M., Bascompte, J., Dupont, Y.L., Jordano, P., 2007. The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America104, 19891–19896.

[51] Peng, G.S., Wu, J., 2016. Optimal network topology for structural robustness based on natural connectivity. Physica A: Statistical Mechanics and its Applications443, 212–220.

[52] Philippot, L., Chenu, C., Kappler, A., Rillig, M.C., Fierer, N., 2024. The interplay between microbial communities and soil properties. Nature Reviews Microbiology22, 226–239.

[53] Qian, F.H., Su, X.M., Zhang, Y., Bao, Y.Y., 2023. Variance of soil bacterial community and metabolic profile in the rhizosphere vs. non-rhizosphere of native plant Rumex acetosa L. from a Sb/As co-contaminated area in China. Journal of Hazardous Materials456, 131681.

[54] Schimel, J.P., Weintraub, M.N., 2003. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology and Biochemistry35, 549–563.

[55] Shade, A., Peter, H., Allison, S.D., Baho, D.L., Berga, M., Bürgmann, H., Huber, D.H., Langenheder, S., Lennon, J.T., Martiny, J.B.H., Matulich, K.L., Schmidt, T.M., Handelsman, J., 2012. Fundamentals of microbial community resistance and resilience. Frontiers in Microbiology3, 417.

[56] Shen, H.J., Zhang, Q.Q., Zhu, S.G., Duan, P.P., Zhang, X., Wu, Z., Xiong, Z.Q., 2021. Organic substitutions aggravated microbial nitrogen limitation and decreased nitrogen-cycling gene abundances in a three-year greenhouse vegetable field. Journal of Environmental Management288, 112379.

[57] Smith, P., Martino, D., Cai, Z.C., Gwary, D., Janzen, H., Kumar, P., McCarl, B., Ogle, S., O'Mara, F., Rice, C., Scholes, B., Sirotenko, O., Howden, M., McAllister, T., Pan, G.X., Romanenkov, V., Schneider, U., Towprayoon, S., Wattenbach, M., Smith, J., 2008. Greenhouse gas mitigation in agriculture. Philosophical Transactions of the Royal Society B: Biological Sciences363, 789–813.

[58] Srinivas, P., Peterson, S.B., Gallagher, L.A., Wang, Y.X., Mougous, J.D., 2024. Beyond genomics in Patescibacteria: A trove of unexplored biology packed into ultrasmall bacteria. Proceedings of the National Academy of Sciences of the United States of America121, e2419369121.

[59] Sun, H.X., Chen, M.M., Wei, L., Xue, P.Y., Zhao, Q.L., Gao, P.P., Geng, L.P., Wen, Q.X., Liu, W.J., 2024. Roots recruited distinct rhizo-microbial communities to adapt to long-term Cd and As co-contaminated soil in wheat-maize rotation. Environmental Pollution342, 123053.

[60] Sun, W.G., Villamil, M.B., Behnke, G.D., Margenot, A.J., 2022. Long-term effects of crop rotation and nitrogen fertilization on phosphorus cycling and balances in loess-derived Mollisols. Geoderma420, 115829.

[61] Tao, J.J., Wang, S.S., Liao, T.H., Luo, H.W., 2021. Evolutionary origin and ecological implication of a unique nif island in free-living Bradyrhizobium lineages. The ISME Journal15, 3195–3206.

[62] Tian, R.M., Ning, D.L., He, Z.L., Zhang, P., Spencer, S.J., Gao, S.H., Shi, W.L., Wu, L.W., Zhang, Y., Yang, Y.F., Adams, B.G., Rocha, A.M., Detienne, B.L., Lowe, K.A., Joyner, D.C., Klingeman, D.M., Arkin, A.P., Fields, M.W., Hazen, T.C., Stahl, D.A., Alm, E.J., Zhou, J.Z., 2020. Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity. Microbiome8, 51.

[63] Tian, W., Wang, L., Li, Y., Zhuang, K.M., Li, G., Zhang, J.B., Xiao, X.J., Xi, Y.G., 2015. Responses of microbial activity, abundance, and community in wheat soil after three years of heavy fertilization with manure-based compost and inorganic nitrogen. Agriculture, Ecosystems & Environment213, 219–227.

[64] Tilman, D., Cassman, K.G., Matson, P.A., Naylor, R., Polasky, S., 2002. Agricultural sustainability and intensive production practices. Nature418, 671–677.

[65] Wang, L., Wang, J., Tang, Z.H., Wang, J.D., Zhang, Y.C., 2024. Long-term organic fertilization reshapes the communities of bacteria and fungi and enhances the activities of C- and P-cycling enzymes in calcareous alluvial soil. Applied Soil Ecology194, 105204.

[66] Wang, X.D., Feng, J.G., Ao, G., Qin, W.K., Han, M.G., Shen, Y.W., Liu, M.L., Chen, Y., Zhu, B., 2023. Globally nitrogen addition alters soil microbial community structure, but has minor effects on soil microbial diversity and richness. Soil Biology and Biochemistry179, 108982.

[67] Wang, X.X., Zhang, W., Liu, Y., Jia, Z.J., Li, H., Yang, Y.F., Wang, D.M., He, H.B., Zhang, X.D., 2021. Identification of microbial strategies for labile substrate utilization at phylogenetic classification using a microcosm approach. Soil Biology and Biochemistry153, 107970.

[68] 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.

[69] Willms, I.M., Rudolph, A.Y., Göschel, I., Bolz, S.H., Schneider, D., Penone, C., Poehlein, A., Schöning, I., Nacke, H., 2020. Globally abundant “Candidatus Udaeobacter” benefits from release of antibiotics in soil and potentially performs trace gas scavenging.. mSphere5, .

[70] Wolińska, A., Kuźniar, A., Zielenkiewicz, U., Izak, D., Szafranek-Nakonieczna, A., Banach, A., Błaszczyk, M., 2017. Bacteroidetes as a sensitive biological indicator of agricultural soil usage revealed by a culture-independent approach. Applied Soil Ecology119, 128–137.

[71] Wright, R.J., Langille, M.G.I., Walker, T.R., 2021. Food or just a free ride? A meta-analysis reveals the global diversity of the Plastisphere. The ISME Journal15, 789–806.

[72] Xie, H.T., Li, J.W., Zhu, P., Peng, C., Wang, J.K., He, H.B., Zhang, X.D., 2014. Long-term manure amendments enhance neutral sugar accumulation in bulk soil and particulate organic matter in a Mollisol. Soil Biology and Biochemistry78, 45–53.

[73] Xu, Q.C., Ling, N., Chen, H., Duan, Y.H., Wang, S., Shen, Q.R., Vandenkoornhuyse, P., 2020. Long-term chemical-only fertilization induces a diversity decline and deep selection on the soil bacteria. mSystems5, e00337–20.

[74] Yang, Z., Dai, H.D., Huang, Y.T., Dong, B., Fu, S.L., Zhang, C.L., Li, X.W., Tan, Y.H., Zhang, X.X., Zhang, X., 2024. Driving mechanisms of soil bacterial α and β diversity under long-term nitrogen addition: subtractive heterogenization based on the environment selection. Geoderma445, 116886.

[75] Zhang, Q., Zhang, Z.Y., Lu, T., Yu, Y.T., Penuelas, J., Zhu, Y.G., Qian, H.F., 2021. Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants. Microbiome9, 196.

[76] Zhang, X.Y., Fang, Q.C., Zhang, T., Ma, W.Q., Velthof, G.L., Hou, Y., Oenema, O., Zhang, F.S., 2020. Benefits and trade-offs of replacing synthetic fertilizers by animal manures in crop production in China: a meta-analysis. Global Change Biology26, 888–900.

[77] Zhang, Y.L., Sun, C.X., Chen, Z.H., Zhang, G.N., Chen, L.J., Wu, Z.J., 2019. Stoichiometric analyses of soil nutrients and enzymes in a Cambisol soil treated with inorganic fertilizers or manures for 26 years. Geoderma353, 382–390.

[78] Zhao, Z.Y., Ma, Y.T., Zhang, A., Chen, Y.M., Zheng, Z.X., Zheng, W., Zhai, B.N., 2023. Response of apple orchard bacteria co-occurrence network pattern to long-term organic fertilizer input. Applied Soil Ecology191, 105035.

[79] Zhou, Z.H., Wang, C.K., Luo, Y.Q., 2020. Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality. Nature Communications11, 3072.

[80] Zhou, Z.H., Zheng, M.H., Xia, J.Y., Wang, C.K., 2022. Nitrogen addition promotes soil microbial beta diversity and the stochastic assembly. Science of the Total Environment806, 150569.

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