Soil pH modulates microbial nitrogen cycling under integrated soil-crop system management across agroecosystems

Faisal Zaman , Ziqi Li , Xiuzheng Fu , Weidong Ma , Xingjie Wu , Jing Tian , Jingjing Peng , Werner Liesack , Zhenling Cui

Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (4) : 250360

PDF (3861KB)
Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (4) : 250360 DOI: 10.1007/s42832-025-0360-9
RESEARCH ARTICLE

Soil pH modulates microbial nitrogen cycling under integrated soil-crop system management across agroecosystems

Author information +
History +
PDF (3861KB)

Abstract

Integrated Soil-Crop System Management (ISSM) has emerged as an effective approach to improve nutrient cycling and crop yield in China. However, its pH-dependent impact on the nitrogen (N) cycling capacity of soil microbiome remains largely unexplored, despite the critical role of pH in shaping microbial processes. Here, we employed comprehensive metagenomic analysis across multiple agricultural sites in China to investigate the effects of ISSM on the N-cycling potential along soil pH gradients, with Farmlandʼs Practice (FP) as a reference. Actinobacteria and Proteobacteria dominated microbial communities across all treatments and pH conditions, accounting for 88%–90% of the total abundance. Microbial alpha diversity remained consistent across the pH gradient, but exhibited significant negative correlations with soil organic carbon and total N. Soil pH showed a strong positive correlation with the abundance of genes associated with nitrification, but showed a negative correlation with denitrification gene abundance. Particularly, ISSM significantly increased the total abundance of nitrogen-cycling genes in the two most acidic soils (LS, GZL), but not in the less acidic (HEB), near-neutral (BD), and alkaline (TY) soils. Relative to FP, the normalized gene abundances associated with denitrification and NH4+ to Org-N were enriched in LS_ISSM, while those related to DNRA, NO3 reduction to ammonia, and nitrification were higher in GZL_ISSM. These results highlight the potential of ISSM to modulate microbial nitrogen cycling and point to the importance of site-specific strategies, particularly in acidic soils, for enhancing nitrogen retention.

Graphical abstract

Keywords

soil pH / nitrogen cycling / metagenomics / soil microbiome

Highlight

● Soil pH positively correlated with the metagenomic abundance of nitrification.

● Soil pH negatively correlated with the metagenomic abundance of denitrification.

● ISSM increased total nitrogen cycle gene abundance in more acidic soils.

Cite this article

Download citation ▾
Faisal Zaman, Ziqi Li, Xiuzheng Fu, Weidong Ma, Xingjie Wu, Jing Tian, Jingjing Peng, Werner Liesack, Zhenling Cui. Soil pH modulates microbial nitrogen cycling under integrated soil-crop system management across agroecosystems. Soil Ecology Letters, 2025, 7(4): 250360 DOI:10.1007/s42832-025-0360-9

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Anderson, M.J., 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics62, 245–253.

[2]

Beeckman, F., Motte, H., Beeckman, T., 2018. Nitrification in agricultural soils: impact, actors and mitigation. Current Opinion in Biotechnology50, 166–173.

[3]

Bolger, A.M., Lohse, M., Usadel, B., 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics30, 2114–2120.

[4]

Buchfink, B., Xie, C., Huson, D.H., 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods12, 59–60.

[5]

Cao, M.M., Li, Y., Zhang, Y.X., Yu, D.B., Uwiragiye, Y., Wang, J., Jing, H., Tang, Q., Qian, Y.F., Elrys, A.S., Cheng, Y., Cai, Z.C., Xu, M.G., Müller, C., 2025. pH threshold in controlling dominant nitrification pathway in acidic soils. Agriculture, Ecosystems & Environment377, 109278.

[6]

Cassim, B.M.A.R., Lisboa, I.P., Besen, M.R., Otto, R., Cantarella, H., Inoue, T.T., Batista, M.A., 2024. Nitrogen: from discovery, plant assimilation, sustainable usage to current enhanced efficiency fertilizers technologies–A review. Revista Brasileira de Ciência do Solo48, e0230037.

[7]

Chen, X.P., Cui, Z.L., Vitousek, P.M., Cassman, K.G., Matson, P.A., Bai, J.S., Meng, Q.F., Hou, P., Yue, S.C., Römheld, V., Zhang, F.S., 2011. Integrated soil–crop system management for food security. Proceedings of the National Academy of Sciences of the United States of America108, 6399–6404.

[8]

Cheng, Y., Elrys, A.S., Merwad, A.R.M., Zhang, H.M., Chen, Z.X., Zhang, J.B., Cai, Z.C., Müller, C., 2022. Global patterns and drivers of soil dissimilatory nitrate reduction to ammonium. Environmental Science & Technology56, 3791–3800.

[9]

Cuhel, J., Šimek, M., Laughlin, R.J., Bru, D., Chèneby, D., Watson, C.J., Philippot, L., 2010. Insights into the effect of soil pH on N2O and N2 emissions and denitrifier community size and activity. Applied and Environmental Microbiology76, 1870–1878.

[10]

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.

[11]

Ding, Y., Huang, X., Li, Y., Liu, H.Y., Zhang, Q.C., Liu, X.M., Xu, J.M., Di, H.J., 2021. Nitrate leaching losses mitigated with intercropping of deep-rooted and shallow-rooted plants. Journal of Soils and Sediments21, 364–375.

[12]

Epp Schmidt, D.J., Pouyat, R., Szlavecz, K., Setälä, H., Kotze, D.J., Yesilonis, I., Cilliers, S., Hornung, E., Dombos, M., Yarwood, S.A., 2017. Urbanization erodes ectomycorrhizal fungal diversity and may cause microbial communities to converge. Nature Ecology & Evolution1, 0123.

[13]

Fang, Y.T., Zhu, W.X., Gundersen, P., Mo, J.M., Zhou, G.Y., Yoh, M., 2009. Large loss of dissolved organic nitrogen from nitrogen-saturated forests in subtropical China. Ecosystems12, 33–45.

[14]

Galloway, J.N., Bleeker, A., Erisman, J.W., 2021. The human creation and use of reactive nitrogen: a global and regional perspective. Annual Review of Environment and Resources46, 255–288.

[15]

Gubry-Rangin, C., Novotnik, B., Mandič-Mulec, I., Nicol, G.W., Prosser, J.I., 2017. Temperature responses of soil ammonia-oxidising archaea depend on pH. Soil Biology and Biochemistry106, 61–68.

[16]

Hoang, H.G., Thuy, B.T.P., Lin, C., Vo, D.V.N., Tran, H.T., Bahari, M.B., Le, V.G., Vu, C.T., 2022. The nitrogen cycle and mitigation strategies for nitrogen loss during organic waste composting: a review. Chemosphere300, 134514.

[17]

Huson, D.H., Beier, S., Flade, I., Górska, A., El-Hadidi, M., Mitra, S., Ruscheweyh, H.J., Tappu, R., 2016. MEGAN community edition – interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Computational Biology12, e1004957.

[18]

Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., Hauser, L.J., 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics11, 119.

[19]

Kaviraj, M., Kumar, U., Chatterjee, S., Parija, S., Padbhushan, R., Nayak, A.K., Gupta, V.V.S.R., 2024. Dissimilatory nitrate reduction to ammonium (DNRA): a unique biogeochemical cycle to improve nitrogen (N) use efficiency and reduce N-loss in rice paddy. Rhizosphere30, 100875.

[20]

Khalifah, S., Foltz, M.E., 2024. The ratio of denitrification end-products were influenced by soil pH and clay content across different texture classes in Oklahoma soils. Frontiers in Soil Science4, 1342986.

[21]

Lai, C.M., Peng, F., Sun, J.B., Zhou, J., Li, C.Y., Xu, X.L., Chen, X.J., You, Q.G., Sun, H.Y., Sun, J., Xue, X., Lambers, H., 2023. Niche differentiation and higher uptake of available nitrogen maintained the productivity of alpine meadow at early degradation. Biology and Fertility of Soils59, 35–49.

[22]

Li, D.H., Liu, C.M., Luo, R.B., Sadakane, K., Lam, T.W., 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics31, 1674–1676.

[23]

Li, Y.Y., Chapman, S.J., Nicol, G.W., Yao, H.Y., 2018. Nitrification and nitrifiers in acidic soils. Soil Biology and Biochemistry116, 290–301.

[24]

Lin, S.X., Liu, Z.J., Wang, Y.C., Li, J.Y., Wang, G.G., Ye, J.H., Wang, H.B., He, H.B., 2022. Soil metagenomic analysis on changes of functional genes and microorganisms involved in nitrogen-cycle processes of acidified tea soils. Frontiers in Plant Science13, 998178.

[25]

Liu, Z., Gao, J., Gao, F., Dong, S.T., Liu, P., Zhao, B., Zhang, J.W., 2018. Integrated agronomic practices management improve yield and nitrogen balance in double cropping of winter wheat–summer maize. Field Crops Research221, 196–206.

[26]

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.

[27]

Luo, M., Moorhead, D.L., Ochoa-Hueso, R., Mueller, C.W., Ying, S.C., Chen, J., 2022. Nitrogen loading enhances phosphorus limitation in terrestrial ecosystems with implications for soil carbon cycling. Functional Ecology36, 2845–2858.

[28]

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.

[29]

Murphy, J., Riley, J.P., 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta27, 31–36.

[30]

Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Oksanen, M.J., 2013. Package ‘vegan’. Community ecology package, version2, 1–295.

[31]

Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Borman, T., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, H.B.A., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M.O., Lahti, L., Martino, C., McGlinn, D., Ouellette, M.H., Cunha, E.R., Smith, T., Stier, A., Ter Braak, C.J.F., Weedon, J., 2022. Vegan: community ecology package. Version 2.6-4. R Packages.

[32]

Olsen, S.R., Sommers, L.E., 1982. Phosphorus. In: Page, A.L., ed. Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties. 2nd ed. Madison: American Society of Agronomy403–430.

[33]

Ouyang, Y., Evans, S.E., Friesen, M.L., Tiemann, L.K., 2018. Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: a meta-analysis of field studies. Soil Biology and Biochemistry127, 71–78.

[34]

Pandey, C.B., Kumar, U., Kaviraj, M., Minick, K.J., Mishra, A.K., Singh, J.S., 2020. DNRA: a short-circuit in biological N-cycling to conserve nitrogen in terrestrial ecosystems. Science of the Total Environment738, 139710.

[35]

Peng, J.J., Wegner, C.E., Bei, Q.C., Liu, P.F., Liesack, W., 2018. Metatranscriptomics reveals a differential temperature effect on the structural and functional organization of the anaerobic food web in rice field soil. Microbiome6, 169.

[36]

Qiu, Y.P., Zhang, Y., Zhang, K.C., Xu, X.Y., Zhao, Y.F., Bai, T.S., Zhao, Y.X., Wang, H., Sheng, X.J., Bloszies, S., Gillespie, C.J., He, T.Q., Wang, Y., Chen, H.H., Guo, L.J., Song, H., Ye, C.L., Wang, Y., Woodley, A., Guo, J.H., Cheng, L., Bai, Y.F., Zhu, Y.G., Hallin, S., Firestone, M.K., Hu, S.J., 2024. Intermediate soil acidification induces highest nitrous oxide emissions. Nature Communications15, 2695.

[37]

Saghaï, A., Pold, G., Jones, C.M., Hallin, S., 2023. Phyloecology of nitrate ammonifiers and their importance relative to denitrifiers in global terrestrial biomes. Nature Communications14, 8249.

[38]

Sakin, E., Yanardağ, H.İ., Fırat, Z., Çelik, A., Beyyavaş, V., Cun, S., 2024. Some indicators for the assessment of soil health: a mini review. MAS Journal of Applied Sciences9, 297–310.

[39]

Saleh-Lakha, S., Shannon, K.E., Henderson, S.L., Goyer, C., Trevors, J.T., Zebarth, B.J., Burton, D.L., 2009. Effect of pH and temperature on denitrification gene expression and activity in Pseudomonas mandelii. Applied and Environmental Microbiology75, 3903–3911.

[40]

Scarlett, K., Denman, S., Clark, D.R., Forster, J., Vanguelova, E., Brown, N., Whitby, C., 2021. Relationships between nitrogen cycling microbial community abundance and composition reveal the indirect effect of soil pH on oak decline. The ISME Journal15, 623–635.

[41]

Shi, W.C., He, Z.M., Lu, J.H., Wang, L.F., Guo, J.H., Qiu, S., Ge, S.J., 2025. Response of nitrifiers to gradually increasing pH conditions in a membrane nitrification bioreactor: microbial dynamics and alkali-resistant mechanism. Water Research268, 122567.

[42]

Singh, S., Tripathi, D.K., Singh, S., Sharma, S., Dubey, N.K., Chauhan, D.K., Vaculík, M., 2017. Toxicity of aluminium on various levels of plant cells and organism: a review. Environmental and Experimental Botany137, 177–193.

[43]

Wan, W.J., Tan, J.D., Wang, Y., Qin, Y., He, H.M., Wu, H.Q., Zuo, W.L., He, D.L., 2020. Responses of the rhizosphere bacterial community in acidic crop soil to pH: changes in diversity, composition, interaction, and function. Science of the Total Environment700, 134418.

[44]

Wang, R.Z., Bicharanloo, B., Hou, E.Q., Jiang, Y., Dijkstra, F.A., 2022. Phosphorus supply increases nitrogen transformation rates and retention in soil: a global meta-analysis. Earth’s Future10, e2021EF002479.

[45]

Wang, S.Y., Zhu, G.B., Zhuang, L., Li, Y.X., Liu, L., Lavik, G., Berg, M., Liu, S.T., Long, X.E., Guo, J.H., Jetten, M.S.M., Kuypers, M., Li, F.B., Schwark, L., Yin, C.Q., 2020. Anaerobic ammonium oxidation is a major N-sink in aquifer systems around the world. The ISME Journal14, 151–163.

[46]

Wang, Z., Zhao, X.X., Sun, Y.F., Liu, W., Zhao, G.Q., Dang, Z.H., 2024. Advancing sustainable agriculture: the role of integrated soil-crop management in maize production. Frontiers in Environmental Science12, 1426956.

[47]

Wannicke, N., Frey, C., Law, C.S., Voss, M., 2018. The response of the marine nitrogen cycle to ocean acidification. Global Change Biology24, 5031–5043.

[48]

Wu, G., Liu, B., Zhao, M.J., Liu, L., Wei, S.J., Yuan, M.M., Wang, J.B., Chen, X.P., Wang, X.Z., Sun, Y.X., 2024. Integrated soil–crop system management promotes sustainability of intensive vegetable production in plastic shed systems: a case study in the Yangtze River Basin, China. Agronomy14, 807.

[49]

Wu, X.J., Liu, Y., Shang, Y.W., Liu, D., Liesack, W., Cui, Z.L., Peng, J.J., Zhang, F.S., 2022. Peat-vermiculite alters microbiota composition towards increased soil fertility and crop productivity. Plant and Soil470, 21–34.

[50]

Wu, X.J., Peng, J.J., Malik, A.A., Peng, Z.H., Luo, Y., Fan, F.L., Lu, Y.H., Wei, G.H., Delgado-Baquerizo, M., Liesack, W., Jiao, S., 2025. A global relationship between genome size and encoded carbon metabolic strategies of soil bacteria. Ecology Letters28, e70064.

[51]

Xiong, R.N., He, X.H., Gao, N., Li, Q., Qiu, Z.J., Hou, Y.X., Shen, W.S., 2024. Soil pH amendment alters the abundance, diversity, and composition of microbial communities in two contrasting agricultural soils. Microbiology Spectrum12, e04165–23.

[52]

Yang, Y., Chen, X.L., Liu, L.X., Li, T., Dou, Y.X., Qiao, J.B., Wang, Y.Q., An, S.S., Chang, S.X., 2022. Nitrogen fertilization weakens the linkage between soil carbon and microbial diversity: a global meta‐analysis. Global Change Biology28, 6446–6461.

[53]

Yu, N.N., Liu, J.A., Ren, B.Z., Zhao, B., Liu, P., Gao, Z., Zhang, J.W., 2022. Long-term integrated soil-crop management improves soil microbial community structure to reduce GHG emission and increase yield. Frontiers in Microbiology13, 1024686.

[54]

Zhang, F.S., Cui, Z.L., Zhang, W.F., 2014. Managing nutrient for both food security and environmental sustainability in China: an experiment for the world. Frontiers of Agricultural Science and Engineering1, 53–61.

[55]

Zhang, P., Li, C.L., Xie, X.H., Gao, Q., Zhang, J.J., Wang, L.C., 2019. Integrated soil-crop system management increases phosphorus concentrations and bioavailability in a Primosol. Journal of Soil Science and Plant Nutrition19, 357–367.

[56]

Zhang, X.M., Liu, W., Schloter, M., Zhang, G.M., Chen, Q.S., Huang, J.H., Li, L.H., Elser, J.J., Han, X.G., 2013. Response of the abundance of key soil microbial nitrogen-cycling genes to multi-factorial global changes. PLoS One8, e76500.

[57]

Zhong, Y.Q.W., Yan, W.M., Canisares, L.P., Wang, S., Brodie, E.L., 2023. Alterations in soil pH emerge as a key driver of the impact of global change on soil microbial nitrogen cycling: evidence from a global meta-analysis. Global Ecology and Biogeography32, 145–165.

[58]

Zhou, J., Zheng, Y.L., Hou, L.J., An, Z.R., Chen, F.Y., Liu, B.L., Wu, L., Qi, L., Dong, H.P., Han, P., Yin, G.Y., Liang, X., Yang, Y., Li, X.F., Gao, D.Z., Li, Y., Liu, Z.F., Bellerby, R., Liu, M., 2023. Effects of acidification on nitrification and associated nitrous oxide emission in estuarine and coastal waters. Nature Communications14, 1380.

RIGHTS & PERMISSIONS

Higher Education Press

AI Summary AI Mindmap
PDF (3861KB)

Supplementary files

supplementary material

316

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/