Elevated plant nitrogen suppresses post-senescence decomposition: A novel mechanism in nitrogen-enriched ecosystems

Abstract

The nitrogen (N) input can exert a dual effect on litter decomposition, depending on the litter quality. Additionally, increased N input alters plant nutrient composition, which directly impacts plant residue decomposition. However, this effect remains understudied, particularly in grassland ecosystems. We obtained two types of Leymus chinensis litter (low-N and high-N) from a long-term N addition experiment. A 730-day litter decomposition experiment was conducted to examine mass loss, nutrient release, stoichiometric changes, and microbial community dynamics. The results show that N addition increased litter mass loss by approximately 10.55%, and the mass loss of low-N litter increased by 10.14%. Furthermore, acid-unhydrolyzable residue accumulated over time, with greater accumulation in high-N litter, which may be a key factor underlying the slower decomposition of high-N litter. Another key factor may be the persistently high N:P ratio in high-N litter during decomposition, potentially making it more susceptible to P limitation. Our findings highlight that changes in litter quality under exogenous nutrient inputs play a key role in regulating decomposition, offering insights to improve predictive models of litter decomposition under changing nutrient inputs.

Graphical abstract

Keywords

grassland / litter decomposition / acid-unhydrolyzable residue / Basidiomycota / stoichiometry

Highlight

	● Nitrogen addition promoted litter decomposition in semi-arid grasslands.
	● Decomposition of high-nitrogen litter was inhibited.
	● N:P ratios in low-N litter remained stable throughout decomposition.
	● Fungal/bacterial intra-kingdom interactions were mainly positive.
	● These findings can improve predictive models of litter decomposition under changing nutrient inputs.

References

[1] Allison, S.D., 2005. Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecology Letters8, 626–635.

[2] Almagro, M., Maestre, F.T., Martínez-López, J., Valencia, E., Rey, A., 2015. Climate change may reduce litter decomposition while enhancing the contribution of photodegradation in dry perennial Mediterranean grasslands. Soil Biology and Biochemistry90, 214–223.

[3] Berg, B., Erhagen, B., Johansson, M.B., Nilsson, M., Stendahl, J., Trum, F., Vesterdal, L., 2015. Manganese in the litter fall-forest floor continuum of boreal and temperate pine and spruce forest ecosystems – A review. Forest Ecology and Management358, 248–260.

[4] Berg, B., Liu, C.J., Laskowski, R., Davey, M., 2013. Relationships between nitrogen, acid-unhydrolyzable residue, and climate among tree foliar litters. Canadian Journal of Forest Research43, 103–107.

[5] Berg, B., Matzner, E., 1997. Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environmental Reviews5, 1–25.

[6] Berg, B., McClaugherty, C., 2020a. Changes in substrate composition during decomposition. In: Berg, B., McClaugherty, C., eds. Plant Litter: Decomposition, Humus Formation, Carbon Sequestration. 4th ed. Cham: Springer101–128.

[7] Berg, B., McClaugherty, C., 2020b. Initial litter chemical composition. In: Berg, B., McClaugherty, C., eds. Plant Litter: Decomposition, Humus Formation, Carbon Sequestration. 4th ed. Cham: Springer67–100.

[8] Berg, B., McClaugherty, C., 2020c. Role of chemical constituents in regulating decay rates and stable fractions: effects of initial and changing chemical composition on decomposition and organic matter accumulation. In: Berg, B., McClaugherty, C., eds. Plant Litter: Decomposition, Humus Formation, Carbon Sequestration. 4th ed. Cham: Springer129–163.

[9] Brabcová, V., Nováková, M., Davidová, A., Baldrian, P., 2016. Dead fungal mycelium in forest soil represents a decomposition hotspot and a habitat for a specific microbial community. New Phytologist210, 1369–1381.

[10] Brown, M.E., Chang, M.C.Y., 2014. Exploring bacterial lignin degradation. Current Opinion in Chemical Biology19, 1–7.

[11] Challacombe, J.F., Hesse, C.N., Bramer, L.M., Mccue, L.A., Lipton, M., Purvine, S., Nicora, C., Gallegos-Graves, L.V., Porras-Alfaro, A., Kuske, C.R., 2019. Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis. BMC Genomics20, 976.

[12] Chang, Q., Wang, L., Ding, S.W., Xu, T.T., Li, Z.Q., Song, X.X., Zhao, X., Wang, D.L., Pan, D.F., 2018. Grazer effects on soil carbon storage vary by herbivore assemblage in a semi-arid grassland. Journal of Applied Ecology55, 2517–2526.

[13] Coûteaux, M.M., Bottner, P., Berg, B., 1995. Litter decomposition, climate and liter quality. Trends in Ecology & Evolution10, 63–66.

[14] Cui, Y.X., Moorhead, D.L., Wang, X.X., Xu, M.Z., Wang, X., Wei, X.M., Zhu, Z.K., Ge, T.D., Peng, S.S., Zhu, B., Zhang, X.C., Fang, L.C., 2022. Decreasing microbial phosphorus limitation increases soil carbon release. Geoderma419, 115868.

[15] Davey, M.P., Berg, B., Emmett, B.A., Rowland, P., 2007. Decomposition of oak leaf litter is related to initial litter Mn concentrations. Canadian Journal of Botany85, 16–24.

[16] de Boer, W., Folman, L.B., Summerbell, R.C., Boddy, L., 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiology Reviews29, 795–811.

[17] de Gonzalo, G., Colpa, D.I., Habib, M.H.M., Fraaije, M.W., 2016. Bacterial enzymes involved in lignin degradation. Journal of Biotechnology236, 110–119.

[18] Faust, K., Raes, J., 2012. Microbial interactions: from networks to models. Nature Reviews Microbiology10, 538–550.

[19] Fog, K., 1988. The effect of added nitrogen on the rate of decomposition of organic matter. Biological Reviews63, 433–462.

[20] Friedman, J., Alm, E.J., 2012. Inferring correlation networks from genomic survey data. PLoS Computational Biology8, e1002687.

[21] Gao, X.X., Dong, S.K., Xu, Y.D., Li, Y., Li, S., Wu, S., Shen, H., Liu, S.L., Fry, E.L., 2021. Revegetation significantly increased the bacterial-fungal interactions in different successional stages of alpine grasslands on the Qinghai-Tibetan Plateau. CATENA205, 105385.

[22] Giachetti, V.I., Vivanco, L., 2025. Magnesium addition increases microbial metabolic efficiency during decomposition of Patagonian leaf litter. Plant and Soil507, 749–761.

[23] Gill, A.L., Adler, P.B., Borer, E.T., Buyarski, C.R., Cleland, E.E., D'Antonio, C.M., Davies, K.F., Gruner, D.S., Harpole, W.S., Hofmockel, K.S., Macdougall, A.S., McCulley, R.L., Melbourne, B.A., Moore, J.L., Morgan, J.W., Risch, A.C., Schütz, M., Seabloom, E.W., Wright, J.P., Yang, L.H., Hobbie, S.E., 2022. Nitrogen increases early-stage and slows late-stage decomposition across diverse grasslands. Journal of Ecology110, 1376–1389.

[24] Güsewell, S., 2004. N:P ratios in terrestrial plants: variation and functional significance. New Phytologist164, 243–266.

[25] Güsewell, S., Freeman, C., 2005. Nutrient limitation and enzyme activities during litter decomposition of nine wetland species in relation to litter N:P ratios. Functional Ecology19, 582–593.

[26] Güsewell, S., Gessner, M.O., 2009. N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Functional Ecology23, 211–219.

[27] Haq, I.U., Zhang, M.Z., Yang, P., van Elsas, J.D., 2014. The interactions of bacteria with fungi in soil: emerging concepts. Advances in Applied Microbiology89, 185–215.

[28] Hart, S.C., 1999. Nitrogen transformations in fallen tree boles and mineral soil of an old-growth forest. Ecology80, 1385–1394.

[29] Hättenschwiler, S., Jørgensen, H.B., 2010. Carbon quality rather than stoichiometry controls litter decomposition in a tropical rain forest. Journal of Ecology98, 754–763.

[30] Herzog, C., Hartmann, M., Frey, B., Stierli, B., Rumpel, C., Buchmann, N., Brunner, I., 2019. Microbial succession on decomposing root litter in a drought-prone Scots pine forest. The ISME Journal13, 2346–2362.

[31] Hobbie, S.E., Eddy, W.C., Buyarski, C.R., Adair, E.C., Ogdahl, M.L., Weisenhorn, P., 2012. Response of decomposing litter and its microbial community to multiple forms of nitrogen enrichment. Ecological Monographs82, 389–405.

[32] Hoppe, B., Kahl, T., Karasch, P., Wubet, T., Bauhus, J., Buscot, F., Krüger, D., 2014. Network analysis reveals ecological links between N-fixing bacteria and wood-decaying fungi. PLoS One9, e88141.

[33] Hou, S.L., Freschet, G.T., Yang, J.J., Zhang, Y.H., Yin, J.X., Hu, Y.Y., Wei, H.W., Han, X.G., Lü, X.T., 2018. Quantifying the indirect effects of nitrogen deposition on grassland litter chemical traits. Biogeochemistry139, 261–273.

[34] Hou, S.L., Hättenschwiler, S., Yang, J.J., Sistla, S., Wei, H.W., Zhang, Z.W., Hu, Y.Y., Wang, R.Z., Cui, S.Y., Lü, X.T., Han, X.G., 2021. Increasing rates of long-term nitrogen deposition consistently increased litter decomposition in a semi-arid grassland. New Phytologist229, 296–307.

[35] Hu, S., Wang, B.T., Li, T.H., Bu, S., Jin, C.Z., Jin, L., Ruan, H.H., Shin, K.S., Jin, F.J., 2025. Successional patterns of microbial communities across various stages of leaf litter decomposition in poplar plantations. Frontiers in Microbiology16, 1628355.

[36] Huang, Y., Wang, L., Wang, D.L., Zeng, D.H., Li, Y.X., Liu, J., Wang, Y., 2018. Foraging responses of sheep to plant spatial micro-patterns can cause diverse associational effects of focal plant at individual and population levels. Journal of Animal Ecology87, 863–873.

[37] Innangi, M., Schenk, M.K., d’Alessandro, F., Pinto, S., Menta, C., Papa, S., Fioretto, A., 2015. Field and microcosms decomposition dynamics of European beech leaf litter: influence of climate, plant material and soil with focus on N and Mn. Applied Soil Ecology93, 88–97.

[38] Ji, Y.L., Li, Q., Tian, K., Yang, J.B., Hu, H.J., Yuan, L.H., Lu, W.S., Yao, B., Tian, X.J., 2020. Effect of sodium amendments on the home-field advantage of litter decomposition in a subtropical forest of China. Forest Ecology and Management468, 118148.

[39] Jia, Y.Y., Kong, X.S., Weiser, M.D., Lv, Y.N., Akbar, S., Jia, X.Q., Tian, K., He, Z.H., Lin, H., Bei, Z.L., Tian, X.J., 2015. Sodium limits litter decomposition rates in a subtropical forest: additional tests of the sodium ecosystem respiration hypothesis. Applied Soil Ecology93, 98–104.

[40] Kaiser, C., Franklin, O., Dieckmann, U., Richter, A., 2014. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecology Letters17, 680–690.

[41] Kaspari, M., Garcia, M.N., Harms, K.E., Santana, M., Wright, S.J., Yavitt, J.B., 2008. Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecology Letters11, 35–43.

[42] Keeler, B.L., Hobbie, S.E., Kellogg, L.E., 2009. Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems12, 1–15.

[43] Knorr, M., Frey, S.D., Curtis, P.S., 2005. Nitrogen additions and litter decomposition: a meta-analysis. Ecology86, 3252–3257.

[44] Kominoski, J.S., Rosemond, A.D., Benstead, J.P., Gulis, V., Maerz, J.C., Manning, D.W.P., 2015. Low-to-moderate nitrogen and phosphorus concentrations accelerate microbially driven litter breakdown rates. Ecological Applications25, 856–865.

[45] Layeghifard, M., Hwang, D.M., Guttman, D.S., 2017. Disentangling interactions in the microbiome: a network perspective. Trends in Microbiology25, 217–228.

[46] Li, Z.L., Peng, Q., Dong, Y.S., Guo, Y., 2022. The influence of increased precipitation and nitrogen deposition on the litter decomposition and soil microbial community structure in a semiarid grassland. Science of the Total Environment844, 157115.

[47] Li, Z.M., Wu, J.F., Han, Q., Nie, K.Y., Xie, J.N., Li, Y.F., Wang, X.Y., Du, H.B., Wang, D.L., Liu, J.S., 2021. Nitrogen and litter addition decreased sexual reproduction and increased clonal propagation in grasslands. Oecologia195, 131–144.

[48] Liao, C.J., Huang, W.J., Wells, J., Zhao, R.Y., Allen, K., Hou, E.Q., Huang, X., Qiu, H., Tao, F., Jiang, L.F., Aguilos, M., Lin, L., Huang, X.M., Luo, Y.Q., 2022. Microbe-iron interactions control lignin decomposition in soil. Soil Biology and Biochemistry173, 108803.

[49] Liu, D., Keiblinger, K.M., Leitner, S., Mentler, A., Zechmeister-Boltenstern, S., 2016. Is there a convergence of deciduous leaf litter stoichiometry, biochemistry and microbial population during decay. Geoderma272, 93–100.

[50] Lovett, G.M., Arthur, M.A., Crowley, K.F., 2016. Effects of calcium on the rate and extent of litter decomposition in a northern hardwood forest. Ecosystems19, 87–97.

[51] Malik, A.A., Chowdhury, S., Schlager, V., Oliver, A., Puissant, J., Vazquez, P.G.M., Jehmlich, N., von Bergen, M., Griffiths, R.I., Gleixner, G., 2016. Soil fungal: bacterial ratios are linked to altered carbon cycling. Frontiers in Microbiology7, 1247.

[52] Manning, P., Saunders, M., Bardgett, R.D., Bonkowski, M., Bradford, M.A., Ellis, R.J., Kandeler, E., Marhan, S., Tscherko, D., 2008. Direct and indirect effects of nitrogen deposition on litter decomposition. Soil Biology and Biochemistry40, 688–698.

[53] Manzoni, S., Trofymow, J.A., Jackson, R.B., Porporato, A., 2010. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecological Monographs80, 89–106.

[54] Meidute, S., Demoling, F., Bååth, E., 2008. Antagonistic and synergistic effects of fungal and bacterial growth in soil after adding different carbon and nitrogen sources. Soil Biology and Biochemistry40, 2334–2343.

[55] Moore, T.R., Trofymow, J.A., Prescott, C.E., Fyles, J., Titus, B.D., 2006. Patterns of carbon, nitrogen and phosphorus dynamics in decomposing foliar litter in canadian forests. Ecosystems9, 46–62.

[56] Mooshammer, M., Wanek, W., Schnecker, J., Wild, B., Leitner, S., Hofhansl, F., Blöchl, A., Hämmerle, I., Frank, A.H., Fuchslueger, L., Keiblinger, K.M., Zechmeister-Boltenstern, S., Richter, A., 2012. Stoichiometric controls of nitrogen and phosphorus cycling in decomposing beech leaf litter. Ecology93, 770–782.

[57] Olson, J.S., 1963. Energy storage and the balance of producers and decomposers in ecological systems. Ecology44, 322–331.

[58] Peng, Y., Yang, J.X., Seabloom, E.W., Sardans, J., Peñuelas, J., Zhang, H.Y., Wei, C.Z., Han, X.G., 2025. Multiple nutrient additions homogenize multidimensional plant stoichiometry in a meadow steppe. Global Change Biology31, e70123.

[59] Preston, C.M., Nault, J.R., Trofymow, J.A., 2009. Chemical changes during 6 years of decomposition of 11 litters in some canadian forest sites. Part 2. ¹³C abundance, solid-state ¹³C NMR spectroscopy and the meaning of “Lignin”. Ecosystems12, 1078–1102.

[60] Purahong, W., Wubet, T., Lentendu, G., Schloter, M., Pecyna, M.J., Kapturska, D., Hofrichter, M., Krüger, D., Buscot, F., 2016. Life in leaf litter: novel insights into community dynamics of bacteria and fungi during litter decomposition. Molecular Ecology25, 4059–4074.

[61] R Core Team, 2025. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

[62] Robbins, C.J., Manning, D.W.P., Halvorson, H.M., Norman, B.C., Eckert, R.A., Pastor, A., Dodd, A.K., Jabiol, J., Bastias, E., Gossiaux, A., Mehring, A.S., 2023. Nutrient and stoichiometry dynamics of decomposing litter in stream ecosystems: a global synthesis. Ecology104, e4060.

[63] Romaní, A.M., Fischer, H., Mille-Lindblom, C., Tranvik, L.J., 2006. Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. Ecology87, 2559–2569.

[64] Rudnick, M.B., van Veen, J.A., de Boer, W., 2015. Baiting of rhizosphere bacteria with hyphae of common soil fungi reveals a diverse group of potentially mycophagous secondary consumers. Soil Biology and Biochemistry88, 73–82.

[65] Sachs, J.L., Hollowell, A.C., 2012. The origins of cooperative bacterial communities. mBio3, e00099–12.

[66] Schneider, T., Keiblinger, K.M., Schmid, E., Sterflinger-Gleixner, K., Ellersdorfer, G., Roschitzki, B., Richter, A., Eberl, L., Zechmeister-Boltenstern, S., Riedel, K., 2012. Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. The ISME Journal6, 1749–1762.

[67] Shabtai, I.A., Wilhelm, R.C., Schweizer, S.A., Höschen, C., Buckley, D.H., Lehmann, J., 2023. Calcium promotes persistent soil organic matter by altering microbial transformation of plant litter. Nature Communications14, 6609.

[68] Spohn, M., Berg, B., 2023. Import and release of nutrients during the first five years of plant litter decomposition. Soil Biology and Biochemistry176, 108878.

[69] Strassmann, J.E., Gilbert, O.M., Queller, D.C., 2011. Kin discrimination and cooperation in microbes. Annual Review of Microbiology65, 349–367.

[70] Sun, T., Dong, L.L., Zhang, Y.Y., Hättenschwiler, S., Schlesinger, W.H., Zhu, J.J., Berg, B., Adair, E.C., Fang, Y.T., Hobbie, S.E., 2024. General reversal of N-decomposition relationship during long-term decomposition in boreal and temperate forests. Proceedings of the National Academy of Sciences of the United States of America121, e2401398121.

[71] Torres, P.A., Abril, A.B., Bucher, E.H., 2005. Microbial succession in litter decomposition in the semi-arid Chaco woodland. Soil Biology and Biochemistry37, 49–54.

[72] Trum, F., Titeux, H., Cornelis, J.T., Delvaux, B., 2011. Effects of manganese addition on carbon release from forest floor horizons. Canadian Journal of Forest Research41, 643–648.

[73] Voříšková, J., Baldrian, P., 2013. Fungal community on decomposing leaf litter undergoes rapid successional changes. The ISME Journal7, 477–486.

[74] Wang, C.Q., Kuzyakov, Y., 2024. Mechanisms and implications of bacterial–fungal competition for soil resources. The ISME Journal18, wrae073.

[75] Wang, H.C., Wang, H., Crowther, T.W., Isobe, K., Reich, P.B., Tateno, R., Shi, W.Y., 2024. Metagenomic insights into inhibition of soil microbial carbon metabolism by phosphorus limitation during vegetation succession. ISME Communications4, ycae128.

[76] Wang, L., Delgado-Baquerizo, M., Wang, D.L., Isbell, F., Liu, J., Feng, C., Liu, J.S., Zhong, Z.W., Zhu, H., Yuan, X., Chang, Q., Liu, C., 2019. Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proceedings of the National Academy of Sciences of the United States of America116, 6187–6192.

[77] Watts, S.C., Ritchie, S.C., Inouye, M., Holt, K.E., 2019. FastSpar: rapid and scalable correlation estimation for compositional data. Bioinformatics35, 1064–1066.

[78] Wen, T., Xie, P.H., Yang, S.D., Niu, G.Q., Liu, X.Y., Ding, Z.X., Xue, C., Liu, Y.X., Shen, Q.R., Yuan, J., 2022. ggClusterNet: an R package for microbiome network analysis and modularity-based multiple network layouts. iMeta1, e32.

[79] Wu, W.C., Wang, F., Xia, A.Q., Zhang, Z.J., Wang, Z.S., Wang, K., Dong, J.F., Li, T., Wu, Y.B., Che, R.X., Li, L.F., Niu, S.L., Hao, Y.B., Wang, Y.F., Cui, X.Y., 2022. Meta-analysis of the impacts of phosphorus addition on soil microbes. Agriculture, Ecosystems & Environment340, 108180.

[80] Xu, X.F., Thornton, P.E., Post, W.M., 2013. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Global Ecology and Biogeography22, 737–749.

[81] Xu, Z.W., Yu, G.R., Zhang, X.Y., Ge, J.P., He, N.P., Wang, Q.F., Wang, D., 2015. The variations in soil microbial communities, enzyme activities and their relationships with soil organic matter decomposition along the northern slope of Changbai Mountain. Applied Soil Ecology86, 19–29.

[82] Yue, K., Yang, W.Q., Peng, C.H., Peng, Y., Zhang, C., Huang, C.P., Tan, Y., Wu, F.Z., 2016. Foliar litter decomposition in an alpine forest meta-ecosystem on the eastern Tibetan Plateau. Science of the Total Environment566–567, 279–287.

[83] Zechmeister-Boltenstern, S., Keiblinger, K.M., Mooshammer, M., Peñuelas, J., Richter, A., Sardans, J., Wanek, W., 2015. The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecological Monographs85, 133–155.

[84] Zheng, H.P., Yang, T.J., Bao, Y.Z., He, P.P., Yang, K.M., Mei, X.L., Wei, Z., Xu, Y.C., Shen, Q.R., Banerjee, S., 2021. Network analysis and subsequent culturing reveal keystone taxa involved in microbial litter decomposition dynamics. Soil Biology and Biochemistry157, 108230.

[85] Zheng, P., Zhao, R.N., Jiang, L.C., Yang, G.J., Wang, Y.L., Wang, R.Z., Han, X.G., Ning, Q.S., 2023. Increasing nitrogen addition rates suppressed long-term litter decomposition in a temperate meadow steppe. Journal of Plant Ecology16, rtac078.

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