High variation of fungal communities and associated potential plant pathogens induced by long-term addition of N fertilizers rather than P, K fertilizers: A case study in a Mollisol field

Abstract

• Fungal communities were more sensitive to N fertilizers than P, K fertilizers.

• More harmonious and stable fungal network induced by P, K fertilizers.

• N fertilizers induced lower fungal community resistance with detriments on crop yields.

Nitrogen (N), phosphate (P), and potassium (K) are the three most important nutrients applied into agricultural soils, but the impacts of their single or combined application on soil fungal community structure and stability are still open questions. Using qPCR and Illumina Miseq sequencing, the variation of soil fungal communities in response to long-term addition of N, P, or K fertilization alone and their combinations in a Mollisol field was investigated in this study. In addition, the fungal community resistance indices and network structure were studied. Results showed that N fertilizations (N, NK, NP and NPK treatments) rather than P, K fertilizations (P, K and PK treatments) significantly increased fungal abundance, but decreased fungal diversity and shifted fungal community structures when compared to non-fertilization (NoF). Additionally, N fertilization treatments presented lower resistance of fungal communities to environment disturbances than those of P, K fertilization treatments. More numbers and higher abundances of changed fungal taxa at the genus and OTU levels were induced by N fertilizations rather than by addition of P, K fertilizers. In addition, N fertilizations induced a more changeable fungal network and complex pathogenic subnetwork with many positive interactions among responding plant pathogens (RP, the changeable plant pathogens induced by fertilizers addition compared to NoF) when compared to P, K fertilizations. These RP directly and negatively influenced fungal community resistance examined by structural equation modeling (SEM), which were indirectly detrimental to soybean yields. Our findings revealed that addition of N fertilizers significantly disturbed fungal communities and promoted pathogenic interactions, and provided insights into the optimization of fertilization strategies toward agricultural sustainability.

Graphical abstract

Keywords

N fertilizations / P, K fertilizations / Fungal communities / Responding taxa / Network interaction / Mollisol

References

[1] Aguilar-Trigueros, C.A., Hempel, S., Powell, J.R., Anderson, I.C., Antonovics, J., Bergmann, J., Cavagnaro, T.R., Chen, B., Hart, M.M., Klironomos, J., Petermann, J.S., Verbruggen, E., Veresoglou, S.D., Rillig, M.C., 2015. Branching out, towards a trait-based understanding of fungal ecology. Fungal Biology Reviews 29, 34–41

[2] Allison, S.D., Martiny, J.B.H., 2008. Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the United States of America 105, 11512–11519

[3] Banerjee, S., Kirkby, C.A., Schmutter, D., Bissett, A., Kirkegaard, J.A., Richardson, A.E., 2016. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biology & Biochemistry 97, 188–198

[4] Barberán, A., Bates, S.T., Casamayor, E.O., Fierer, N., 2012. Using network analysis to explore co-occurrence. ISME Journal 6, 343–351

[5] Becker, J., Eisenhauer, N., Scheu, S., Jousset, A., 2012. Increasing antagonistic interactions cause bacterial communities to collapse at high diversity. Ecology Letters 15, 468–474

[6] Bonn, W.G., Cappellini, R.A., 1970. Sporulation of Gibberella zeae. III. Carbon and nitrogen nutrition on growth and macroconidium production. Canadian Journal of Botany 48, 1335–1337

[7] Cabrerizo, M.J., Medina-Sánchez, J.M., Villar-Argaiz, M., Carrillo, P., 2019. Interplay between resistance and resilience governs the stability of a freshwater microbial food web under multiple stressors. Science of the Total Environment 691, 908–918

[8] Camenzind, T., Hättenschwiler, S., Treseder, K.K., Lehmann, A., Rillig, M.C., 2018. Nutrient limitation of soil microbial process in tropical forests. Ecological Monographs 88, 4–21

[9] Chen, W., Zhou, H., Wu, Y., Wang, J., Zhao, Z., Li, Y., Qiao, L., Chen, K., Liu, G., Xue, S., 2020. Direct and indirect influences of long-term fertilization on microbial carbon and nitrogen cycles in an alpine grassland. Soil Biology & Biochemistry 149, 107922

[10] Churchill, A.C.L., Dunkle, L.D., Silbert, W., Kennedy, K.J., Macko, V., 2001. Differential synthesis of peritoxins and precursors by pathogenic strains of the fungus Periconia circinata. Applied and Environmental Microbiology 67, 5721–5728

[11] Deng, Y., Jiang, Y.H., Yang, Y., He, Z., Luo, F., Zhou, J., 2012. Molecular ecological network analyses. BMC Bioinformatics 13, 113

[12] Edgar, R.C., 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998

[13] Ellouze, W., Taheri, A.E., Bainard, L.D., Yang, C., Bazghaleh, N., Navarro-Borrell, A., Hanson, K., Hamel, C., 2014. Soil fungal resources in annual cropping systems and their potential for management. BioMed Research International 2014, 531824–531815

[14] Fan, K., Delgado-Baquerizo, M., Guo, X., Wang, D., Zhu, Y., Chu, H., 2019. Microbial resistance promotes plant production in a four-decade nutrient fertilization experiment. Soil Biology & Biochemistry 141, 107679

[15] Fuhrman, J.A., 2009. Microbial community structure and its functional implications. Nature 459, 193–199

[16] Geisseler, D., Scow, K.M., 2014. Long-term of effects of mineral fertilizers on soil microorganisms–A review. Soil Biology & Biochemistry 75, 54–63

[17] Girvan, M.S., Campbell, C.D., Killham, K., Prosser, J.L., Glover, L.A., 2005. Bacterial diversity promotes community stability and functional resilience after perturbation. Environmental Microbiology 7, 301–313

[18] Grace, J.B., 2006. Structural Equation Modeling and Natural Systems. Cambridge University Press, Cambridge

[19] Hayden, H.L., Drake, J., Imhof, M., Oxley, A.P.A., Norng, S., Mele, P.M., 2010. The abundance of nitrogen cycle genes amoA and nifH depends on land-uses and soil types in South-Eastern Australia. Soil Biology & Biochemistry 42, 1774–1783

[20] Hu, X., Liu, J., Wei, D., Zhou, B., Chen, X., Jin, J., Liu, X., Wang, G., 2019. Long-term application of nitrogen, not phosphate or potassium, significantly alters the diazotrophic community compositions and structures in a mollisol in northeast China. Research in Microbiology 170, 147–155

[21] Hu, X., Liu, J., Wei, D., Zhu, P., Cui, X., Zhou, B., Chen, X., Jin, J., Liu, X., Wang, G., 2017. Effects of over 30-year of different fertilization regimes on fungal community compositions in the black soils of northeast China. Agriculture, Ecosystems & Environment 248, 113–122

[22] 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 Letters 11, 35–43.

[23] Koike, Y., Cai, H.J., Higashiyama, K., Fujikawa, S., Park, E.Y., 2001. Effect of consumed carbon to nitrogen ratio on mycelial morphology and arachidonic acid production in cultures of Mortierella alpina. Journal of Bioscience and Bioengineering 91, 382–389

[24] Lajeunesse, M.J., 2011. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92, 2049–2055

[25] Li, J.H., Cheng, B.H., Zhang, R., Li, W.J., Shi, X.M., Han, Y.W., Ye, L.F., Ostle, N.J., Bardgett, R.D., 2021. Nitrogen and phosphorus additions accelerate decomposition of slow carbon pool and lower total soil organic carbon pool in alpine meadows. Land Degradation & Development 32, 1761–1772

[26] Lin, X., Feng, Y., Zhang, H., Chen, R., Wang, J., Zhang, J., Chu, H., 2012. Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environmental Science & Technology 46, 5764–5771

[27] Liu, L., Gundersen, P., Zhang, T., Mo, J., 2012a. Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biology & Biochemistry 44, 31–38

[28] Liu, X., Burras, C.L., Kravchenko, Y.S., Duran, A., Huffman, T., Morras, H., Studdert, G., Cruse, R.M., Yuan, X., 2012b. Overview of Mollisols in the world: distribution, land use and management. Canadian Journal of Soil Science 92, 383–402

[29] Liu, Y., Shi, G., Mao, L., Cheng, G., Jiang, S., Ma, X., An, L., Du, G., Johnson, N.C., Feng, H., 2012c. Direct and indirect influences of 8yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytologist 194, 523–535

[30] Lu, X., Mao, Q., Gilliam, F.S., Luo, Y., Mo, J., 2014. Nitrogen deposition contributes to soil acidification in tropical ecosystems. Global Change Biology 20, 3790–3801

[31] Luizão, F.J., Luizão, R.C.C., Proctor, J., 2007. Soil acidity and nutrient deficiency in central Amazonian heath forest soils. Plant Ecology 192, 209–224

[32] Lunardi, L.W., Aquino, V.R., Zimerman, R.A., Goldani, L.Z., 2006. Epidemiology and outcome of Rhodotorula fungemia in a tertiary care hospital. Clinical Infectious Diseases 43, e60–e63

[33] Ma, S., Chen, G., Tang, W., Xing, A., Chen, X., Xiao, W., Zhou, L., Zhu, J., Li, Y., Zhu, B., Fang, J., 2021. Inconsistent responses of soil microbial community structure and enzyme activity to nitrogen and phosphorus additions in two trophic forests. Plant and Soil 460, 453–468

[34] Ma, S., Shan, J., Yan, X., 2017. N₂O emissions dominated by fungi in an intensively managed vegetable field converted from wheat-rice rotation. Applied Soil Ecology 116, 23–29

[35] Malinowski, D.P., Belesky, D.P., 2000. Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Science 40, 923–940

[36] Malinowski, D.P., Belesky, D.P., 2006. Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassland Science 52, 1–14

[37] Mirzaee, M., Asgari, B., Zare, R., Mohammadi, M., 2010. Association of Microascus cirrosus (Microascaceae, Ascomycetes) with brown leaf spot of Pistachio in Iran. Plant Disease 94, 642

[38] Morriën, E., Hannula, S.E., Snoek, L.B., Helmsing, N.R., Zweers, H., de Hollander, M., Soto, L.R., Bouffaud, M.L., Buée, M., Dimmers, W., Duyts, H., Geisen, S., Girlanda, M., Griffiths, R.I., Jørgensen, H.B., Jensen, J., Plassart, P., Redecker, D., Schmelz, R.M., Schmidt, O., Thomson, B.B., Tisserant, E., Uroz, S., Winding, A., Bailey, M.J., Bonkowski, M., Faber, J.H., Martin, F., Lemanceau, P., de Boer, W., van Veen, J.A., van der Putten, W.H., 2017. Soil networks become more connected and take up more carbon as nature restoration progresses. Nature Communications 8, 14349

[39] Morrison, E.W., Frey, S.D., Sadowsky, J.J., van Diepen, L.T.A., Thomas, W.K., Pringle, A., 2016. Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest. Fungal Ecology 23, 48–57

[40] Mujica, M.I., Pérez, M.F., Jakalski, M., Martos, F., Selosse, M.A., 2020. Soil P reduces mycorrhizal colonization while favors fungal pathogens: observational and experimental evidence in Bipinnula (Orchidaceae). FEMS Microbiology Ecology 96, fiaa178.

[41] Nguyen, N.H., Song, Z., Bates, S.T., Branco, S., Tedersoo, L., Menke, J., Schilling, J.S., Kennedy, P.G., 2016. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20, 241–248

[42] Ning, Q., Chen, L., Jia, Z., Zhang, C., Ma, D., Li, F., Zhang, J., Li, D., Han, X., Cai, Z., Huang, S., Liu, W., Zhu, B., Li, Y., 2020. Multiple long-term observations reveal a strategy for soil pH-dependent fertilization and fungal communities in support of agricultural production. Agriculture, Ecosystems & Environment 293, 106837

[43] Orwin, K.H., Wardle, D.A., 2004. New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biology & Biochemistry 36, 1907–1912

[44] Osorio Vega, N.W., Habte, M., León Peláez, J.D., 2015. Effectiveness of a rock phosphate solubilizing fungus to increase soil solution phosphate impaired by the soil phosphate sorption capacity. Revista Facultad Nacional de Agronomía 68, 7627–7636

[45] Peay, K.G., Baraloto, C., Fine, P.V., 2013. Strong coupling of plant and fungal community structure across western Amazonian rainforests. ISME Journal 7, 1852–1861

[46] Pioli, R.N., Mozzoni, L., Morandi, E.N., 2004. First report of pathogenic association between Fusarium graminearum and soybean. Plant Disease 88, 220

[47] Qiao, C., Penton, C.R., Xiong, W., Liu, C., Wang, R., Liu, Z., Xu, X., Li, R., Shen, Q., 2019. Reshaping the rhizosphere microbiome by bio-organic amendment to enhance crop yield in a maize-cabbage rotation system. Applied Soil Ecology 142, 136–146

[48] Saikkonen, K., Lehtonen, P., Helander, M., Koricheva, J., Faeth, S.H., 2006. Model systems in ecology: dissecting the endophyte-grass literature. Trends in Plant Science 11, 428–433

[49] Shen, J., Zhang, L., Guo, J., Ray, J.L., He, J., 2010. Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China. Applied Soil Ecology 46, 119–124

[50] Shi, S., Nuccio, E.E., Shi, Z.J., He, Z., Zhou, J., Firestone, M.K., 2016. The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages. Ecology Letters 19, 926–936

[51] Song, G., Chen, R., Xiang, W., Yang, F., Zheng, S., Zhang, J., Zhang, J., Lin, X., 2015. Contrasting effects of long-term fertilization on the community of saprotrophic fungi and arbuscular mycorrhizal fungi in a sandy loam soil. Plant, Soil and Environment 61, 127–136

[52] Spohn, M., Pötsch, E.M., Eichorst, S.A., Woebken, D., Wanek, W., Richter, A., 2016. Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biology & Biochemistry 97, 168–175

[53] Steiner, C., Teixeira, W.G., Lehmann, J., Nehls, T., de Macêdo, J.L.V., Blum, W.E.H., Zech, W., 2007. Long term effects of manure, charcoal and mineral fertilization on crop production and fertility on a highly weathered Central Amazonian upland soil. Plant and Soil 291, 275–290

[54] Su, J.Q., Ding, L., Xue, K., Yao, H., Quensen, J., Bai, S., Wei, W., Wu, J., Zhou, J., Tiedje, J.M., Zhu, Y., 2014. Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Molecular Ecology 24, 136–150

[55] Sun, R., Dsouza, M., Gilbert, J.A., Guo, X., Wang, D., Guo, Z., Ni, Y., Chu, H., 2016. Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environmental Microbiology 18, 5137–5150

[56] Tagawa, M., Tamaki, H., Manome, A., Koyama, O., Kamagata, Y., 2010. Isolation and characterization of antagonistic fungi against potato scab pathogens from potato field soils. FEMS Microbiology Letters 305, 136–142

[57] Tamayo-Velez, A., Osorio, N.W., 2017. Co-inoculation with an arbuscular mycorrhizal fungus and a phosphate-solubilizing fungus promotes the plant growth and phosphate uptake of avocado plantlets in a nursery. Botany 95, 539–545

[58] Tang, W., Chen, D., Phillips, O.L., Liu, X., Zhou, Z., Li, Y., Xi, D., Zhu, F., Fang, J., Zhang, L., Lin, M., Wu, J., Fang, Y., 2018. Effects of long-term increased N deposition on tropical montane forest soil N₂ and N₂O emissions. Soil Biology & Biochemistry 126, 194–203

[59] Tautges, N.E., Sullivan, T.S., Reardon, C.L., Burke, I.C., 2016. Soil microbial diversity and activity linked to crop yield and quality in a dryland organic wheat production system. Applied Soil Ecology 108, 258–268

[60] Treseder, K.K., 2008. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters 11, 1111–1120

[61] Turner, B.L., Wright, S.J., 2014. The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117, 115–130

[62] Ullah, S., Ai, C., Ding, W., Jiang, R., Zhao, S., Zhang, J., Zhou, W., Hou, Y., He, P., 2019. The response of soil fungal diversity and community composition to long-term fertilization. Applied Soil Ecology 140, 35–41

[63] Wagg, C., Jansa, J., Schmid, B., van der Heijden, M.G.A., 2011. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecology Letters 14, 1001–1009

[64] Wang, H., Li, X., Li, X., Wang, J., Li, X., Guo, Q., Yu, Z., Yang, T., Zhang, H., 2020. Long-term no-tillage and different residue amounts alter soil microbial community composition and increase the risk of maize root rot in northeast China. Soil & Tillage Research 196, 104452

[65] Wang, Y., Ji, H., Hu, Y., Wang, R., Rui, J., Guo, S., 2018. Different selectivity in fungal communities between manure and mineral fertilizers, a study in an alkaline soil after 30 years fertilization. Frontiers in Microbiology 9, 2613

[66] Wen, Y.C., Li, H.Y., Lin, Z.A., Zhao, B.Q., Sun, Z.B., Yuan, L., Xu, J.K., Li, Y.Q., 2020. Long-term fertilization alters soil properties and fungal community composition in fluvo-aquic soil of the North China plain. Scientific Reports 10, 7198

[67] White, T., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: Innis, M.A., ed. PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, pp. 315–322.

[68] Wirth, F., Goldani, L.Z., 2012. Epidemiology of Rhodotorula: An emerging pathogen. Interdisciplinary Perspectives on Infectious Diseases 2012, 465717

[69] Wohl, D.L., Arora, S., Gladstone, J.R., 2004. Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment. Ecology 85, 1534–1540

[70] Xiang, X., Liu, J., Zhang, J., Li, D., Xu, C., Kuzyakov, Y., 2020. Divergence in fungal abundance and community structure between soils under long-term mineral and organic fertilization. Soil & Tillage Research 196, 104491

[71] Xiong, W., Li, R., Ren, Y., Liu, C., Zhao, Q., Wu, H., Jousset, A., Shen, Q., 2017. Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biology & Biochemistry 107, 198–207

[72] Yao, R., Yang, J., Zhu, W., Li, H., Yin, C., Jing, Y., Wang, X., Xie, W., Zhang, X., 2021. Impact of crop cultivation, nitrogen and fulvic acid on soil fungal community structure in salt-affected alluvial fluvo-aquic soil. Plant and Soil 2021, 1–20.

[73] Ye, G.P., Lin, Y.X., Luo, J.F., Di, H.J., Lindsey, S., Liu, D.Y., Fan, J.B., Ding, W.X., 2020. Responses of soil fungal diversity and community composition to long-term fertilization: field experiment in an acidic Ultisol and literature synthesis. Applied Soil Ecology 145, 103305

[74] Yu, Z., Hu, X., Wei, D., Liu, J., Zhou, B., Jin, J., Liu, X., Wang, G., 2019. Long-term inorganic fertilizer use influences bacterial communities in Mollisols of Northeast China based on high-throughput sequencing and network analyses. Archives of Agronomy and Soil Science 65, 1331–1340

[75] Zhang, T., Chen, H.Y.H., Ruan, H., 2018. Global negative effects of nitrogen deposition on soil microbes. ISME Journal 13, 1817–1825

[76] Zhao, A., Liu, L., Chen, B., Fu, W., Xie, W., Xu, T., Zhang, W., Ye, Q., Feng, H., Fu, S., 2020. Soil fungal community is more sensitive to nitrogen deposition than increased rainfall in a mixed deciduous forest of China. Soil Ecology Letters 2, 20–32

[77] Zhou, J., Deng, Y., Luo, F., He, Z., Tu, Q., Zhi, X., 2010. Functional molecular ecological networks. mBio 1, 1592–1601

[78] Zhou, J., Deng, Y., Zhang, P., Xue, K., Liang, Y., Van Nostrand, J.D., Yang, Y., He, Z., Wu, L., Stahl, D.A., Hazen, T.C., Tiedje, J.M., Arkin, A.P., 2014. Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proceedings of the National Academy of Sciences of the United States of America 111, 836–845

[79] Zhou, Z., Wang, C., Zheng, M., Jiang, L., Luo, Y., 2017. Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biology & Biochemistry 115, 433–441

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