Plant diversity is coupled with soil fungal diversity in a natural temperate steppe of northeastern China

Highlights

• Soil fungal community composition varied significantly between study sites.

• Plant species richness (PSR) contributed most to the variation in soil fungi community.

• Both α and β diversity of soil fungi coupled well with that of plant.

• Plant diversity can predict soil fungal diversity in the temperate steppe of northeastern China.

Abstract

Soil fungi and aboveground plant play vital functions in terrestrial ecosystems, while the relationship between aboveground plant diversity and the unseen soil fungal diversity remains unclear. We established 6 sites from the west to the east of the temperate steppe that vary in plant diversity (plant species richness: 7-32) to explore the relationship between soil fungal diversity and aboveground plant diversity. Soil fungal community was characterized by applying 18S rRNA gene sequencing using MiSeq PE300 and aligned with Silva 132 database. As a result, soil fungal community was predominately composed of species within the Ascomycota (84.36%), Basidiomycota (7.22%) and Mucoromycota (6.44%). Plant species richness occupied the largest explanatory power in structuring soil fungal community (19.05%–19.78%). The alpha (α) diversity of the whole soil fungi and Ascomycota showed a hump-backed pattern with increasing plant species richness, and the beta (β) diversity of the whole soil fungi and Ascomycota increased with increasing plant β diversity. Those results indicated that soil fungi and external resources were well balanced at the 20-species level of plant and the sites were more distinct in the composition of their plant communities also harbored more distinct soil fungal communities. Thus, plant diversity could predict both soil fungal α and β diversity in the temperate steppe of northeastern China.

Graphical abstract

Keywords

Temperate steppe / Sequencing / Plant diversity / Soil fungal diversity

References

[1] Anderson, M.J., Ellingsen, K.E., Mcardle, B.H., 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters 9, 683–693

[2] Andersson, S., Nilsson, S.I., 2001. Influence of pH and temperature on microbial activity, substrate availability of soil-solution bacteria and leaching of dissolved organic carbon in a mor humus. Soil Biology & Biochemistry 33, 1181–1191

[3] Bahram, M., Polme, S., Koljalg, U., Zarre, S., Tedersoo, L., 2012. Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytologist 193, 465–473

[4] Bezemer, T.M., Lawson, C.S., Hedlund, K., Edwards, A.R., Brook, A.J., Igual, J.M., Mortimer, S.R., Van der Putten, W.H., 2006. Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. Journal of Ecology 94, 893–904

[5] Blanchet, F.G., Legendre, P., Borcard, D., 2008. Forward selection of explanatory variables. Ecology 89, 2623–2632

[6] Borneman, J., Hartin, R.J., 2000. PCR primers that amplify fungal rRNA genes from environmental samples. Applied and Environmental Microbiology 66, 4356–4360

[7] Broeckling, C.D., Broz, A.K., Bergelson, J., Manter, D.K., Vivanco, J.M., 2008. Root exudates regulate soil fungal community composition and diversty. Applied and Environmental Microbiology 74, 738–744

[8] Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Tumbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336

[9] Carrara, J.E., Walter, C.A., Hawkins, J.S., Peterjohn, W.T., Averill, C., Brzostek, E.R., 2018. Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization. Global Change Biology 24, 2721–2734

[10] Chase, M.W., Reveal, J.L., 2009. A phylogenetic classification of the land plants to accompany APG III. Botanical Journal of the Linnean Society 161, 122–127

[11] Chen, W.Q., Xu, R., Wu, Y.T., Chen, J., Zhang, Y.J., Hu, T.M., Yuan, X.P., Zhou, L., Tan, T.Y., Fan, J.R., 2018. Plant diversity is coupled with beta not alpha diversity of soil fungal communities following N enrichment in a semi-arid grassland. Soil Biology & Biochemistry 116, 388–398

[12] Chen, Y.L., Xu, T.L., Veresoglou, S.D., Hu, H.W., Hao, Z.P., Hu, Y.J., Liu, L., Deng, Y., Rillig, M.C., Chen, B.D., 2017. Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biology & Biochemistry 110, 12–21

[13] Curlevski, N.J.A., Xu, Z.H., Anderson, I.C., Cairney, J.W.G., 2010. Soil fungal communities differ in native mixed forest and adjacent Araucaria cunninghamii plantations in subtropical Australia. Journal of Soils and Sediments 10, 1278–1288

[14] Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Jeffries, T.C., Gaitan, J.J., Encinar, D., Berdugo, M., Campbell, C.D., Singh, B.K., 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nature Communications 7, 10541

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

[16] Eisenhauer, N., Bessler, H., Engels, C., Gleixner, G., Habekost, M., Milcu, A., Partsch, S., Sabais, A.C.W., Scherber, C., Steinbeiss, S., Weigelt, A., Weisser, W.W., Scheu, S., 2010. Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91, 485–496

[17] Eom, A.H., Hartnett, D.C., Wilson, G.W.T., 2000. Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122, 435–444

[18] Frey, S.D., Lee, J., Melillo, J.M., Six, J., 2013. The temperature response of soil microbial efficiency and its feedback to climate. Nature Climate Change 3, 395–398

[19] Gao, C., Zhang, Y., Shi, N.N., Zheng, Y., Chen, L., Wubet, T., Bruelheide, H., Both, S., Buscot, F., Ding, Q., Erfmeier, A., Kuehn, P., Nadrowski, K., Scholten, T., Guo, L.D., 2015. Community assembly of ectomycorrhizal fungi along a subtropical secondary forest succession. New Phytologist 205, 771–785

[20] Guo, X., Feng, J., Shi, Z., Zhou, X., Yuan, M., Tao, X., Hale, L., Yuan, T., Wang, J., Qin, Y., Zhou, A., Fu, Y., Wu, L., He, Z., Van Nostrand, J.D., Ning, D., Liu, X., Luo, Y., Tiedje, J.M., Yang, Y., Zhou, J., 2018. Climate warming leads to divergent succession of grassland microbial communities. Nature Climate Change 8, 813–818

[21] 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

[22] He, J.Z., Xu, Z.H., Hughes, J., 2005. Analyses of soil fungal communities in adjacent natural forest and hoop pine plantation ecosystems of subtropical Australia using molecular approaches based on 18S rRNA genes. FEMS Microbiology Letters 247, 91–100

[23] Hodge, A., Campbell, C.D., Fitter, A.H., 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413, 297–299

[24] Hooper, D.U., Bignell, D.E., Brown, V.K., Brussaard, L., Dangerfield, J.M., Wall, D.H., Wardle, D.A., Coleman, D.C., Giller, K.E., Lavelle, P., Van der Putten, W.H., De Ruiter, P.C., Rusek, J., Silver, W.L., Tiedje, J.M., Wolters, V., 2000. Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: Patterns, mechanisms, and feedbacks. Bioscience 50, 1049–1061

[25] Hossain, M.Z., Sugiyama, S., 2011. Influences of plant litter diversity on decomposition, nutrient mineralization and soil microbial community structure. Grassland Science 57, 72–80

[26] Kondoh, M., 2001. Unifying the relationships of species richness to productivity and disturbance. Proceedings of the Royal Society of London 268, 269–271

[27] Kou, Y.P., Li, J.B., Wang, Y.S., Li, C.A., Tu, B., Yao, M.J., Li, X.Z., 2017. Scale-dependent key drivers controlling methane oxidation potential in Chinese grassland soils. Soil Biology & Biochemistry 111, 104–114

[28] Kuzyakov, Y., Xu, X., 2013. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist 198, 656–669

[29] Lange, M., Habekost, M., Eisenhauer, N., Roscher, C., Bessler, H., Engels, C., Oelmann, Y., Scheu, S., Wilcke, W., Schulze, E.D., Gleixner, G., 2014. Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland. PLoS One 9, e96182

[30] Li, G.X., Xu, G.R., Shen, C.C., Tang, Y., Zhang, Y.X., Ma, K.M., 2016. Contrasting elevational diversity patterns for soil bacteria between two ecosystems divided by the treeline. Science China. Life Sciences 59, 1177–1186

[31] Li, H., Zhang, J.H., Hu, H.F., Chen, L.Y., Zhu, Y.K., Shen, H.H., Fang, J.Y., 2017. Shift in soil microbial communities with shrub encroachment in Inner Mongolia grasslands, China. European Journal of Soil Biology 79, 40–47

[32] Liu, D., Liu, G., Chen, L., Wang, J., Zhang, L., 2018. Soil pH determines fungal diversity along an elevation gradient in Southwestern China. Science China. Life Sciences 61, 718–726

[33] Liu, Z.F., Liu, G.H., Fu, B.J., Zheng, X.X., 2008. Relationship between plant species diversity and soil microbial functional diversity along a longitudinal gradient in temperate grasslands of Hulunbeir, Inner Mongolia, China. Ecological Research 23, 511–518

[34] Ma, L., Guo, C., Lu, X., Yuan, S., Wang, R., 2015. Soil moisture and land use are major determinants of soil microbial community composition and biomass at a regional scale in northeastern China. Biogeosciences 12, 2585–2596

[35] Moll, J., Goldmann, K., Kramer, S., Hempel, S., Kandeler, E., Marhan, S., Ruess, L., Kruger, D., Buscot, F., 2015. Resource type and availability regulate fungal communities along arable soil profiles. Microbial Ecology 70, 390–399

[36] Ochoa-Hueso, R., Collins, S.L., Delgado-Baquerizo, M., Hamonts, K., Pockman, W.T., Sinsabaugh, R.L., Smith, M.D., Knapp, A.K., Power, S.A., 2018. Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents. Global Change Biology 24, 2818–2827

[37] Oksanen, J., Kindt, R., Legendre, P., O'Hara, B. 2007. vegan: Community Ecology Package. R package version 2.0–6.

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

[39] Pec, G.J., Karst, J., Taylor, D.L., Cigan, P.W., Erbilgin, N., Cooke, J.E.K., Simard, S.W., Cahill, J.F. Jr, 2017. Change in soil fungal community structure driven by a decline in Ectomycorrhizal fungi following a mountain pine beetle (Dendroctonus ponderosae) outbreak. New Phytologist 213, 864–873

[40] Pellissier, L., Niculita-Hirzel, H., Dubuis, A., Pagni, M., Guex, N., Ndiribe, C., Salamin, N., Xenarios, I., Goudet, J., Sanders, I.R., Guisan, A., 2014. Soil fungal communities of grasslands are environmentally structured at a regional scale in the Alps. Molecular Ecology 23, 4274–4290

[41] Pennekamp, F., Pontarp, M., Tabi, A., Altermatt, F., Alther, R., Choffat, Y., Fronhofer, E.A., Ganesanandamoorthy, P., Garnier, A., Griffiths, J.I., Greene, S., Horgan, K., Massie, T.M., Machler, E., Palamara, G.M., Seymour, M., Petchey, O.L., 2018. Biodiversity increases and decreases ecosystem stability. Nature 563, 109–112

[42] Porazinska, D.L., Farrer, E.C., Spasojevic, M.J., de Mesquita, C.P.B., Sartwell, S.A., Smith, J.G., White, C.T., King, A.J., Suding, K.N., Schmidt, S.K., 2018. Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology 99, 1942–1952

[43] Prober, S.M., Leff, J.W., Bates, S.T., Borer, E.T., Firn, J., Harpole, W.S., Lind, E.M., Seabloom, E.W., Adler, P.B., Bakker, J.D., Cleland, E.E., DeCrappeo, N.M., DeLorenze, E., Hagenah, N., Hautier, Y., Hofmockel, K.S., Kirkman, K.P., Knops, J.M.H., La Pierre, K.J., MacDougall, A.S., McCulley, R.L., Mitchell, C.E., Risch, A.C., Schuetz, M., Stevens, C.J., Williams, R.J., Fierer, N., 2015. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecology Letters 18, 85–95

[44] Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, 590–596

[45] R Core Team, 2013. R: a language and environment for statistical computing (Vienna: R Foundatin for Statistical Computing).

[46] Ren, B.H., Hu, Y.M., Chen, B.D., Zhang, Y., Thiele, J., Shi, R.J., Liu, M.A., Bu, R.C., 2018. Soil pH and plant diversity shape soil bacterial community structure in the active layer across the latitudinal gradients in continuous permafrost region of Northeastern China. Scientific Reports 8, 5619

[47] Rottstock, T., Joshi, J., Kummer, V., Fischer, M., 2014. Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95, 1907–1917

[48] Rousk, J., Baath, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal 4, 1340–1351

[49] Scherer-Lorenzen, M., 2008. Functional diversity affects decomposition processes in experimental grasslands. Functional Ecology 22, 547–555

[50] 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

[51] Smith, M.E., Douhan, G.W., Rizzo, D.M., 2007. Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analysis of sporocarps and pooled roots. New Phytologist 174, 847–863

[52] Spehn, E.M., Joshi, J., Schmid, B., Alphei, J., Korner, C., 2000. Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant and Soil 224, 217–230

[53] Tang, X., Zhou, Y., Li, H., Yao, L., Ding, Z., Ma, M., Yu, P., 2020. Remotely monitoring ecosystem respiration from various grasslands along a large-scale east-west transect across northern China. Carbon Balance and Management 15, 6

[54] Tedersoo, L., Bahram, M., Cajthaml, T., Polme, S., Hiiesalu, I., Anslan, S., Harend, H., Buegger, F., Pritsch, K., Koricheva, J., Abarenkov, K., 2016. Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME Journal 10, 346–362

[55] Tedersoo, L., Bahram, M., Polme, S., Koljalg, U., Yorou, N.S., Wijesundera, R., Ruiz, L.V., Vasco-Palacios, A.M., Thu, P.Q., Suija, A., Smith, M.E., Sharp, C., Saluveer, E., Saitta, A., Rosas, M., Riit, T., Ratkowsky, D., Pritsch, K., Poldmaa, K., Piepenbring, M., Phosri, C., Peterson, M., Parts, K., Partel, K., Otsing, E., Nouhra, E., Njouonkou, A.L., Nilsson, R.H., Morgado, L.N., Mayor, J., May, T.W., Majuakim, L., Lodge, D.J., Lee, S.S., Larsson, K.H., Kohout, P., Hosaka, K., Hiiesalu, I., Henkel, T.W., Harend, H., Guo, L.D., Greslebin, A., Grelet, G., Geml, J., Gates, G., Dunstan, W., Dunk, C., Drenkhan, R., Dearnaley, J., De Kesel, A., Dang, T., Chen, X., Buegger, F., Brearley, F.Q., Bonito, G., Anslan, S., Abell, S., Abarenkov, K., 2014. Global diversity and geography of soil fungi. Science 346, 1078–1078

[56] Tedersoo, L., Bahram, M., Toots, M., Diedhiou, A.G., Henkel, T.W., Kjoller, R., Morris, M.H., Nara, K., Nouhra, E., Peay, K.G., Polme, S., Ryberg, M., Smith, M.E., Koljalg, U., 2012. Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Molecular Ecology 21, 4160–4170

[57] Tian, Q.Y., Liu, N.N., Bai, W.M., Li, L.H., Chen, J.Q., Reich, P.B., Yu, Q., Guo, D.L., Smith, M.D., Knapp, A.K., Cheng, W.X., Lu, P., Gao, Y., Yang, A., Wang, T.Z., Li, X., Wang, Z.W., Ma, Y.B., Han, X.G., Zhang, W.H., 2016. A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe. Ecology 97, 65–74

[58] Tu, B., Domene, X., Yao, M.J., Li, C.N., Zhang, S.H., Kou, Y.P., Wang, Y.S., Li, X.Z., 2017. Microbial diversity in Chinese temperate steppe: unveiling the most influential environmental drivers. FEMS Microbiology Ecology 93, 93

[59] Waldrop, M.P., Zak, D.R., Blackwood, C.B., Curtis, C.D., Tilman, D., 2006. Resource availability controls fungal diversity across a plant diversity gradient. Ecology Letters 9, 1127–1135

[60] Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633

[61] Webb, C.O., Donoghue, M.J., 2005. Phylomatic: tree assembly for applied phylogenetics. Molecular Ecology Notes 5, 181–183

[62] Yang, T., Adams, J.M., Shi, Y., He, J.S., Jing, X., Chen, L.T., Tedersoo, L., Chu, H.Y., 2017. Soil fungal diversity in natural grasslands of the Tibetan Plateau: associations with plant diversity and productivity. New Phytologist 215, 756–765

[63] Yao, M.J., Rui, J.P., Niu, H.S., Hedenec, P., Li, J.B., He, Z.L., Wang, J.M., Cao, W.D., Li, X.Z., 2017. The differentiation of soil bacterial communities along a precipitation and temperature gradient in the eastern Inner Mongolia steppe. Catena 152, 47–56

[64] Zak, D.R., Holmes, W.E., White, D.C., Peacock, A.D., Tilman, D., 2003. Plant diversity, soil microbial communities, and ecosystem function: Are there any links? Ecology 84, 2042–2050

[65] Zanne, A.E., Tank, D.C., Cornwell, W.K., Eastman, J.M., Smith, S.A., FitzJohn, R.G., McGlinn, D.J., O’Meara, B.C., Moles, A.T., Reich, P.B., Royer, D.L., Soltis, D.E., Stevens, P.F., Westoby, M., Wright, I.J., Aarssen, L., Bertin, R.I., Calaminus, A., Govaerts, R., Hemmings, F., Leishman, M.R., Oleksyn, J., Soltis, P.S., Swenson, N.G., Warman, L., Beaulieu, J.M., 2014. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92

[66] Zhang, X.F., Zhao, L., Xu, S.J. Jr, Liu, Y.Z., Liu, H.Y., Cheng, G.D., 2013. Soil moisture effect on bacterial and fungal community in Beilu River (Tibetan Plateau) permafrost soils with different vegetation types. Journal of Applied Microbiology 114, 1054–1065

Acknowledgements

This study was supported by the National Key Research and Development Program of China (2016YFC0502100) and the Fundamental Research Funds for the Central Universities, Southwest Minzu University (2020NYBPY07).

Disclosure statement

The authors declare no conflict of interest.

RIGHTS & PERMISSIONS

2021 Higher Education Press