Soil fungal community is more sensitive to nitrogen deposition than increased rainfall in a mixed deciduous forest of China

Abstract

Nitrogen (N) deposition and intensified rainfall can strongly affect soil microbial community, but compared with available studies on bacteria, those on soil fungi are quite limited. Here we carried out a field experiment in a mixed deciduous forest of China to study the influences of increased N deposition and rainfall on soil fungi by using quantitative PCR and high-throughput sequencing method. The results demonstrated that (1) N addition significantly increased fungal abundance and alpha diversity (richness, Shannon index and Invsimpson index), changed fungal community composition at OTU level, and marginally increased the relative abundance of Ascomycota and Zygomycota, while water addition showed no remarkable effects on fungal abundance, biodiversity and community composition. (2) N addition significantly increased the richness of saprotrophic fungi and pathogenic fungi, and the relative abundance of saprotrophic fungi, but water addition only slightly increased the abundance of pathogenic fungi. (3) Fungal composition dissimilarity closely correlated with the disparity of soil parameters as a whole. Soil NH₄⁺-N exhibited strong positive correlation with the richness of pathogenic fungi and mycorrhizal fungi, while both soil moisture and NH₄⁺-N tightly correlated with soil fungal abundance and alpha diversity indices. We concluded that in this N-limited but non-water-limited forest ecosystem, N deposition posed stronger effects on soil fungi than increased rainfall, partially mediated by changes in soil properties.

Keywords

Climate change / Fungi / Functional group / Saprotrophic fungi / Pathogenic fungi / Mycorrhizal fungi

References

[1] Affokpon, A., Coyne, D.L., Lawouin, L., Tossou, C., Dossou Agbèdè, R., Coosemans, J., 2011. Effectiveness of native West African arbuscular mycorrhizal fungi in protecting vegetable crops against root-knot nematodes. Biology and Fertility of Soils 47, 207–217

[2] Aguilar-Trigueros, C.A., Hempel, S., Powell, J.R., Anderson, I.C., Rillig, M.C., 2015. Branching out, towards a trait-based understanding of fungal ecology. Fungal Biology Reviews 29, 34–41

[3] Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402

[4] Anderson, M.J., 2010. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.

[5] Barnes, C.J., van der Gast, C.J., McNamara, N.P., Rowe, R., Bending, G.D., 2018. Extreme rainfall affects assembly of the root-associated fungal community. New Phytologist 220, 1172–1184

[6] Brown, J.R., Blankinship, J.C., Niboyet, A., van Groenigen, K.J., Dijkstra, P., Roux, X.L., Leadley, P.W., Hungate, B.A., 2012. Effects of multiple global change treatments on soil N₂O fluxes. Biogeochemistry 109, 85–100

[7] Butterbach-Bahl, K., Gasche, R., Breuer, L., Papen, H., 1997. Fluxes of NO and N₂O from temperate forest soils, impact of forest type, N deposition and of liming on the NO and N₂O emissions. Nutrient Cycling in Agroecosystems 48, 79–90

[8] Chen, B., Nayuki, K., Kuga, Y., Zhang, X., Wu, S., Ohtomo, R., 2018. Uptake and intraradical immobilization of cadmium by arbuscular mycorrhizal fungi as revealed by a stable isotope tracer and synchrotron radiation μX-ray fluorescence analysis. Microbes and Environments 33, 257–263

[9] Chen, Y.L., Xu, Z.W., Veresoglou, S.D., Yang, G.W., Chen, B.D., 2017. Nitrogen deposition and precipitation induced phylogenetic clustering of arbuscular mycorrhizal fungal communities. Soil Biology & Biochemistry 115, 233–242

[10] Dagenais, T.R.T., Keller, N.P., 2009. Pathogenesis of Aspergillus fumigatus in invasive Aspergillosis. Clinical Microbiology Reviews 22, 447–465

[11] Dean, R.B., Dixon, W.J., 1951. Simplified statistics for small numbers of observations. Analytical Chemistry 23, 636–638

[12] Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 26, 2460–2461

[13] Entwistle, E.M., Zak, D.R., Edwards, I.P., 2013. Long-term experimental nitrogen deposition alters the composition of the active fungal community in the forest floor. Soil Science Society of America Journal 77, 1648–1658

[14] Fierer, N., Bradford, M.A., Jackson, R.B., 2007. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364

[15] Frey, S.D., Six, J., Elliott, E.T., 2003. Reciprocal transfer of carbon and nitrogen by decomposer fungi at the soil-litter interface. Soil Biology & Biochemistry 35, 1001–1004

[16] Galloway, J.N., Dentener, F.J., Capone, D.G., Boyer, E.W., Howarth, R.W., Seitzinger, S.P., Asner, G.P., Cleveland, C.C., Green, P.A., Holland, E.A., Karl, D.M., Michaels, A.F., Porter, J.H., Townsend, A.R., Vörösmarty, C.J., 2004. Nitrogen cycles, past, present, and future. Biogeochemistry 70, 153–226

[17] Gilbert, G.S., Webb, C.O., 2007. Phylogenetic signal in plant pathogen-host range. Proceedings of the National Academy of Sciences of the United States of America 104, 4979–4983

[18] Hawkes, C.V., Kivlin, S.N., Rocca, J.D., Huguet, V., Thomsen, M.A., Suttle, K.B., 2011. Fungal community responses to precipitation. Global Change Biology 17, 1637–1645

[19] He, D., Shen, W., Eberwein, J., Zhao, Q., Ren, L., Wu, Q.L., 2017. Diversity and co-occurrence network of soil fungi are more responsive than those of bacteria to shifts in precipitation seasonality in a subtropical forest. Soil Biology & Biochemistry 115, 499–510

[20] Ho, A., Di Lonardo, D.P., Bodelier, P.L.E., 2017. Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiology Ecology 93, fix006

[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] Huang, Y.Y., Olbrecht, L., Yang, X.X., He, J.S., 2014. Effects of nutrient additions on the arbuscular mycorrhizal fungal colonization in the alpine meadow on the tibetan plateau. Universitatis Pekinensis Acta Scientiarum Naturalium (Beijing Da Xue Xue Bao. Zi Ran Ke Xue Ban) 50, 911–918.

[23] IPCC, 2013. Climate Change 2013, The Physical Science Basis. Working group I contribution to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.

[24] Jumpponen, A., Jones, K.L., 2014. Tallgrass prairie soil fungal communities are resilient to climate change. Fungal Ecology 10, 44–57

[25] Kaisermann, A., Maron, P.A., Beaumelle, L., Lata, J.C., 2015. Fungal communities are more sensitive indicators to non-extreme soil moisture variations than bacterial communities. Applied Soil Ecology 86, 158–164

[26] Keiblinger, K.M., Hall, E.K., Wanek, W., Szukics, U., Hämmerle, I., Ellersdorfer, G., Böck, S., Strauss, J., Sterflinger, K., Richter, A., Zechmeister-Boltenstern, S., 2010. The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiology Ecology 73, 430–440

[27] La Porta, N., Capretti, P., Thomsen, I.M., Kasanen, R., Hietala, A.M., Von Weissenberg, K., 2008. Forest pathogens with higher damage potential due to climate change in Europe. Canadian Journal of Plant Pathology 30, 177–195

[28] Ladau, J., Shi, Y., Jing, X., He, J.S., Chen, L., Lin, X., Fierer, N., Gilbert, J.A., Pollard, K.S., Chu, H., 2018. Existing climate change will lead to pronounced shifts in the diversity of soil prokaryotes. mSystems 3, e00167–e18

[29] Li, Y., Bezemer, T.M., Yang, J., Lü, X., Li, X., Liang, W., Han, X., Li, Q., 2018. Changes in litter quality induced by N deposition alter soil microbial communities. Soil Biology & Biochemistry 130, 33–42

[30] Liu, L., Wang, X., Lajeunesse, M.J., Miao, G., Piao, S., Wan, S., Wu, Y., Wang, Z., Yang, S., Li, P., Deng, M., 2016. A cross-biome synthesis of soil respiration and its determinants under simulated precipitation changes. Global Change Biology 22, 1394–1405

[31] Looby, C.I., Treseder, K.K., 2018. Shifts in soil fungi and extracellular enzyme activity with simulated climate change in a tropical montane cloud forest. Soil Biology & Biochemistry 117, 87–96

[32] Loreau, M., de Mazancourt, C., 2013. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecology Letters 16, 106–115

[33] 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

[34] Magoč, T., Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England) 27, 2957–2963

[35] McGuire, K.L., Fierer, N., Bateman, C., Treseder, K.K., Turner, B.L., 2012. Fungal community composition in neotropical rain forests: the influence of tree diversity and precipitation. Microbial Ecology 63, 804–812

[36] McHugh, T.A., Morrissey, E.M., Mueller, R.C., Gallegos-Graves, V., Kuske, C.R., Reed, S.C., 2017. Bacterial, fungal, and plant communities exhibit no biomass or compositional response to two years of simulated nitrogen deposition in a semiarid grassland. Environmental Microbiology 19, 1600–1611

[37] Meier, C.L., Rapp, J., Bowers, R.M., Silman, M., Fierer, N., 2010. Fungal growth on a common wood substrate across a tropical elevation gradient: temperature sensitivity, community composition, and potential for above-ground decomposition. Soil Biology & Biochemistry 42, 1083–1090

[38] 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

[39] Nguyen, N.H., Song, Z.W., 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

[40] Ni, X., Liao, S., Wu, F., Groffman, P.M., 2019. Short-term precipitation pulses stimulate soil CO₂ emission but do not alter CH₄ and N₂O fluxes in a northern hardwood forest. Soil Biology & Biochemistry 130, 8–11

[41] Nilsson, R.H., Larsson, K.H., Taylor, A.F.S., Bengtsson-Palme, J., Jeppesen, T.S., Schigel, D., Kennedy, P., Picard, K., Glõckner, F.O., Tedersoo, L., Saar, I., Kõljalg, U., Abarenkov, K., 2019. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research 47, D259–D264

[42] Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2013. Vegan: Community Ecology Package. R package version2.0–10.

[43] Olsen, S.R., Cole, C.V., Watanabe, F.S., Dean, L.A., 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939, 1–19.

[44] Paungfoo-Lonhienne, C., Yeoh, Y.K., Kasinadhuni, N.R.P., Lonhienne, T.G.A., Robinson, N., Hugenholtz, P., Ragan, M.A., Schmidt, S., 2015. Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Scientific Reports 5, 8678

[45] Rajala, T., Peltoniemi, M., Pennanen, T., Mäkipää, R., 2012. Fungal community dynamics in relation to substrate quality of decaying Norway spruce ( Picea abies [L.] Karst.) logs in boreal forests. FEMS Microbiology Ecology 81, 494–505

[46] Richardson, M., 2009. The ecology of the Zygomycetes and its impact on environmental exposure. Clinical Microbiology and Infection 15, 2–9

[47] Rosier, C.L., Levia, D.F., Van Stan, J.T., Aufdenkampe, A., Kan, J., 2016. Seasonal dynamics of the soil microbial community structure within the proximal area of tree boles: possible influence of stemflow. European Journal of Soil Biology 73, 108–118

[48] Rosier, C.L., Moore, L.D., Wu, T.H., Van Stan, J.T., 2015a. Forest canopy precipitation partitioning: an important plant trait influencing the spatial structure of the symbiotic soil microbial community. Advances in Botanical Research 75, 215–240

[49] Rosier, C.L., Van Stan, J.T. II, Moore, D.M., Schrom, J.O.S., Wu, T.H., Reichard, J.S., Kan, J.J., 2015b. Forest canopy structural controls over throughfall affect soil microbial community structure in an epiphyte-laden maritime oak stand. Ecohydrology 8, 1459–1470

[50] Rousk, J., Brookes, P.C., Bååth, E., 2010. The microbial PLFA composition as affected by pH in an arable soil. Soil Biology & Biochemistry 42, 516–520

[51] She, W., Bai, Y., Zhang, Y., Qin, S., Feng, W., Sun, Y., Zheng, J., Wu, B., 2018. Resource availability drives responses of soil microbial communities to short-term precipitation and nitrogen addition in a desert shrubland. Frontiers in Microbiology 9, 186

[52] Shi, L., Zhang, H., Liu, T., Mao, P., Zhang, W., Shao, Y., Fu, S., 2018. An increase in precipitation exacerbates negative effects of nitrogen deposition on soil cations and soil microbial communities in a temperate forest. Environmental Pollution 235, 293–301

[53] Smith, S.E., Read, D.J., 2008. Mycorrhizal symbiosis. London: Academic press

[54] Thorn, G., 1997. The fungi in soil. In: Dirk Van Elsas J, Trevors JT, Wellington EMH, eds. Modern Soil Microbiology. New York: Marcel Dekker Inc, 63–127.

[55] Tian, D., Du, E., Jiang, L., Ma, S., Zeng, W., Zou, A., Feng, C., Xu, L., Xing, A., Wang, W., Zheng, C., Ji, C., Shen, H., Fang, J., 2018. Responses of forest ecosystems to increasing N deposition in China: A critical review. Environmental Pollution 243, 75–86

[56] Tian, D., Niu, S., 2015. A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters 10, 024019

[57] Vitousek, P.M., Porder, S., Houlton, B.Z., Chadwick, O.A., 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20, 5–15

[58] Walkley, A., 1947. A critical examination of a rapid method for determining organic carbon in soils-effect of variations in digestion conditions and of inorganic soil constituents. Soil Science 63, 251–264

[59] Wang, C., Liu, D., Bai, E., 2018b. Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biology & Biochemistry 120, 126–133

[60] Wang, Y., Ji, H., Hu, Y., Wang, R., Rui, J., Guo, S., 2018a. 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

[61] Woods, A., Coates, K.D., Hamann, A. 2005. Is an unprecedented dothistroma needle blight epidemic related to climate change? BioScience 55, 761–769

[62] Wu, S., Hu, Y., Zhang, X., Sun, Y., Wu, Z., Li, T., Lv, J., Li, J., Zhang, J., Zheng, L., Huang, L., Chen, B., 2018. Chromium detoxification in arbuscular mycorrhizal symbiosis mediated by sulfur uptake and metabolism. Environmental and Experimental Botany 147, 43–52

[63] Yan, G., Xing, Y., Xu, L., Wang, J., Dong, X., Shan, W., Guo, L., Wang, Q., 2017. Effects of different nitrogen additions on soil microbial communities in different seasons in a boreal forest. Ecosphere 8, e01879

[64] Yao, F., Yang, S., Wang, Z., Wang, X., Ye, J., Wang, X., DeBruyn, J.M., Feng, X., Jiang, Y., Li, H., 2017. Microbial taxa distribution is associated with ecological trophic cascades along an elevation gradient. Frontiers in Microbiology 8, 2071

[65] Zhang, H., Liu, H., Zhao, J., Li, G., Lai, X., Li, J., Wang, H., Yang, D.L., 2018b. Response of soil fungal community structure to nitrogen and water addition in Stipa baicalensis steppe. Acta Ecologica Sinica (Sheng Tai Xue Bao) 38, 195–205.

[66] Zhang, H., Wang, L., Liu, H., Zhao, J., Li, G., Wang, H., Lai, X., Li, J., Xiu, W., Yang, D., 2018a. Nitrogen deposition combined with elevated precipitation is conducive to maintaining the stability of the soil fungal diversity on the Stipa baicalensis steppe. Soil Biology & Biochemistry 117, 135–138

[67] Zhang, W., Shen, W., Zhu, S., Wan, S., Luo, Y., Yan, J., Wang, K., Liu, L., Dai, H., Li, P., Dai, K., Zhang, W., Liu, Z., Wang, F., Kuang, Y., Li, Z., Lin, Y., Rao, X., Li, J., Zou, B., Cai, X., Mo, J., Zhao, P., Ye, Q., Huang, J., Fu, S., 2015. Can canopy addition of nitrogen better illustrate the effect of atmospheric nitrogen deposition on forest ecosystem? Scientific Reports 5, 11245

[68] Zhao, A., Liu, L., Xu, T., Shi, L., Xie, W., Zhang, W., Fu, S., Feng, H., Chen, B., 2018. Influences of canopy nitrogen and water addition on AM fungal biodiversity and community composition in a mixed deciduous forest of China. Frontiers in Plant Science 9, 1842

[69] Zhou, J., Jiang, X., Zhou, B., Zhao, B., Ma, M., Guan, D., Li, J., Chen, S., Cao, F., Shen, D., Qin, J., 2016. Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biology & Biochemistry 95, 135–143

Acknowledgments

We thank Zuojian Zhang for the help in soil sampling. We also thank Minghui Che for the assistance in analysis of soil properties. This study was supported by the National Natural Science Foundation of China (41877050; 31300446; 41401286).

Conflict of intrerest

The authors declare no conflict of interest.

RIGHTS & PERMISSIONS

2020 Higher Education Press