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Nitrogen and water addition regulate soil fungal diversity and co-occurrence networks

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
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Abstract

Purpose

A field experiment was conducted to assess the role of nitrogen (N) and water addition in shaping soil fungal communities and co-occurrence networks in temperate grassland, northern China.

Materials and methods

We measured soil fungal and plant community compositions, and also soil properties including available N, phosphorus, potassium concentrations, soil pH, and soil moisture. Soil fungal co-occurrence networks were constructed using a random matrix theory–based network inference approach.

Results and discussion

Plant species richness was decreased by N addition but increased by water addition, whereas fungal richness was decreased by N addition. The fungal community composition was significantly changed by both N addition and water addition. Soil fungal α diversity and β diversity were explained by a combination of variations in plant species richness and plant functional composition, and also by changes in soil pH via the soil acidification pathway induced by N and water addition. The fungal co-occurrence networks were more complex and clustered under water addition than that in ambient precipitation.

Conclusions

Our results suggested that plant functional composition, plant species richness, and soil acidification should be incorporated into ecosystem models for predicting soil fungal communities under future climate changes in terrestrial ecosystems.

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References

  • Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor A FS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungierecent updates and future perspectives. New Phytol 186: 281–285

  • Archer E (2016) Estimate permutation p-values for importance metrics. R package version 2(1), 5 Retrieved from https://CRAN.R-project.org/package = rfpermute

  • Bao SD (2005) Agricultural chemical analysis of soil. China Agriculture Press, Beijing

    Google Scholar 

  • Bengtsson-Palme J, Ryberg M, Hartmann M et al (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for use in environmental sequencing. Methods Ecol Evol 4:914–919

    Google Scholar 

  • Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278

    CAS  Google Scholar 

  • Breiman L (2001) Machine learning. Random forests 45: 5

  • Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    CAS  Google Scholar 

  • Chen YL, Xu ZW, Hu HW, Hu YJ, Hao ZP, Jiang Y, Chen BD (2013) Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Appl Soil Ecol 68:36–45

    Google Scholar 

  • Chen DM, Lan ZC, Hu SJ, Bai YF (2015) Effects of nitrogen enrichment on belowground communities in grassland: relative role of soil nitrogen availability vs. soil acidification. Soil Biol Biochem 89:99–108

    CAS  Google Scholar 

  • Chen YL, Xu TL, Veresoglou SD, Hu HW, Hao ZP, Hu YJ, Liu L, Deng Y, Rillig MC, Chen BD (2017a) Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biol Biochem 110:12–21

    CAS  Google Scholar 

  • Chen YL, Xu ZW, Xu TL, Veresoglou SD, Yang GW, Chen BD (2017b) Nitrogen deposition and precipitation induced phylogenetic clustering of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 115:233–242

    CAS  Google Scholar 

  • Chen WQ, Xu R, Wu YT, Chen J, Zhang YJ, Hu TM, Yuan XP, Zhou L, Tan TY, Fan JR (2018a) Plant diversity is coupled with beta not alpha diversity of soil fungal communities following N enrichment in a semi-arid grassland. Soil Biol Biochem 116:388–398

    CAS  Google Scholar 

  • Chen WQ, Xu R, Chen J, Yuan XP, Zhou L, Tan TY, Fan JR, Zhang YJ, Hu TM (2018b) Consistent responses of surface- and subsurface soil fungal diversity to N enrichment are mediated differently by acidification and plant community in a semi-arid grassland. Soil Biol Biochem 127:110–119

    CAS  Google Scholar 

  • Clark CM, Tilman D (2008) Loss of plant species after chronic low level nitrogen deposition to prairie grasslands. Nature 451:712–715

    CAS  Google Scholar 

  • Cleland EE, Collins SL, Dickson TL, Farrer EC, Gross KL, Gherardi LA, Hallett LM, Hobbs RJ, Hsu JS, Turnbull L, Suding KN (2013) Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation. Ecology 94:1687–1696

    Google Scholar 

  • Cline LC, Hobbie SE, Madritch MD, Buyarski CR, Tilman D, Cavender-Bares JM (2018) Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem. Ecology 99:204–216

    Google Scholar 

  • de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P, Lumini E, Mason KE, Oliver A, Ostle N, Prosser JI, Thion C, Thomson B, Bardgett RD (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:3033

    Google Scholar 

  • Deng Y, Jiang YH, Yang Y, He ZL, Luo F, Zhou JZ (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113

    Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  Google Scholar 

  • Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10

    Google Scholar 

  • Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550

    CAS  Google Scholar 

  • Fornara DA, Tilman D, Hobbie SE (2009) Linkages between plant functional composition, fine root processes and potential soil N mineralization rates. J Ecol 97:48–56

    CAS  Google Scholar 

  • Frostergård A, Bååth E, Tunlid A (1993) Shift in the structure of soil microbial communities in limed forest as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730

    Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    CAS  Google Scholar 

  • Gardes M, Bruns D (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    CAS  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Google Scholar 

  • Harpole WS, Potts DL, Suding KN (2007) Ecosystem responses to water and nitrogen amendment in a California grassland. Glob Chang Biol 13:2341–2348

    Google Scholar 

  • Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB (2011) Fungal community responses to precipitation. Glob Chang Biol 17:1637–1645

    Google Scholar 

  • IPCC (2013) Climatic change 2013: the physical science basis. Cambridge University Press, Cambridge

    Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    CAS  Google Scholar 

  • Klaubauf S, Inselsbacher E, Zechmeister-Boltenstern S, Wanek W, Gottsberger R, Strauss J, Gorfer M (2010) Molecular diversity of fungal communities in agricultural soils from Lower Austria. Fungal Divers 44:65–75

    Google Scholar 

  • Kong Y (2011) Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics 98:152–153

    CAS  Google Scholar 

  • Layeghifard M, Hwang DM, Guttman DS (2017) Disentangling interactions in the microbiome: a network perspective. Trends Microbiol 25:217–228

    CAS  Google Scholar 

  • Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, La Pierre K, Risch AC, Seabloom EW, Schütz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. PNAS 112:10967–10972

    CAS  Google Scholar 

  • Li H, Yang S, Xu ZW, Yan QY, Li XB, van Nostrand JD, He ZL, Yao F, Han XG, Zhou JZ, Deng Y, Jiang Y (2017) Responses of soil microbial functional genes to global changes are indirectly influenced by aboveground plant biomass variation. Soil Biol Biochem 104:18–29

    CAS  Google Scholar 

  • Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2(3):18–22

    Google Scholar 

  • Liu XJ, Duan L, Mo JM, Du EZ, Shen JL, Lu XK, Zhang Y, Zhou XB, He CE, Zhang FS (2011) Nitrogen deposition and its ecological impact in China: an overview. Environ Pollut 159:2251–2264

    CAS  Google Scholar 

  • Liu XJ, Zhang Y, Han WX, Tang A, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS (2013) Enhanced nitrogen deposition over China. Nature 494:459–462

  • Maestre FT, Quero JL, Gotelli NJ, Escudero A, Ochoa V, Delgado-Baquerizo M, García-Gómez M, Bowker MA, Soliveres S, Escolar C, García-Palacios P, Berdugo M, Valencia E, Gozalo B, Gallardo A, Aguilera L, Arredondo T, Blones J, Boeken B, Bran D, Conceição AA, Cabrera O, Chaieb M, Derak M, Eldridge DJ, Espinosa CI, Florentino A, Gaitán J, Gabriel-Gatica M, Ghiloufi W, Gómez-González S, Gutiérrez JR, Hernández RM, Huang X, Huber-Sannwald E, Jankju M, Miriti M, Monerris J, Mau RL, Morici E, Naseri K, Ospina A, Polo V, Prina A, Pucheta E, Ramírez-Collantes DA, Romão R, Tighe M, Torres-Díaz C, Val J, Veiga JP, Wang D, Zaady E (2012) Plant species richness and ecosystem multifunctionality in global drylands. Science 335:214–218

    CAS  Google Scholar 

  • Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, García-Gómez M, Gallardo A, Ulrich W, Bowker MA, Arredondo T, Barraza-Zepeda C, Bran D, Florentino A, Gaitán J, Gutiérrez JR, Huber-Sannwaldi E, Jankju M, Mau RL, Miriti M, Naseri K, Ospina A, Stavi I, Wang D, Woods NN, Yuan X, Zaady E, Singh BK (2015) Increasing aridity reduces soil microbial diversity and abundance in global drylands. PNAS 112:15684–15689

    CAS  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Google Scholar 

  • Millard P, Singh B (2010) Does grassland vegetation drive soil microbial diversity? Nutr Cycl Agroecosys 88: 147–158

  • Mueller RC, Balasch MM, Kuske CR (2014) Contrasting soil fungal community responses to experimental nitrogen addition using the large subunit rRNA taxonomic marker and cellobiohydrolase I functional marker. Mol Ecol 23:4406–4417

    CAS  Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Funct Ecol 20:241–248

    Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2013) Vegan: community ecology package. R package version 2.0–10. http://CRAN.R-project.org/package=vegan

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    CAS  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org/

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    CAS  Google Scholar 

  • Sorensen PO, Germino MJ, Feris KP (2013) Microbial community responses to 17 years of altered precipitation are seasonally dependent and coupled to co-varying effects of water content on vegetation and soil C. Soil Biol Biochem 64:155–163

    CAS  Google Scholar 

  • Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879

    CAS  Google Scholar 

  • Sun Y, Ding Y (2010) A projection of future changes in summer precipitation and monsoon in East Asia. Sci China Earth Sci 53:284–300

    CAS  Google Scholar 

  • Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, Villarreal Ruiz L, Vasco-Palacios AM, Pham-Quang T, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Poldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Paertel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson KH, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo LD, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, De Kesel A, Tan D, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346:1078

    CAS  Google Scholar 

  • Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, van der Heijden MGA (2019) Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun 10:4841

    Google Scholar 

  • Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135

    Google Scholar 

  • Wang S, Wang XB, Han XG, Deng Y (2018) Higher precipitation strengthens the microbial interactions in semi-arid grassland soils. Glob Ecol Biogeogr 27:570–580

    Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    CAS  Google Scholar 

  • Weltzin JF, Loik ME, Schwinning S, Williams DG, Fay P, Haddad B, Harte J, Huxman TE, Knapp AK, Lin G, Pockman WT, Shaw MR, Small E, Smith MD, Smith SD, Tissue DT, Zak JC (2003) Assessing the response of terrestrial ecosystems to potential changes in precipitation. Bioscience 53:941–952

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc., New York, pp 315–322

    Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag New York. URL http://had.co.nz/ggplot2/book

  • Zeilinger S, Gupta VK, Dahms TES, Silva RN, Singh HB, Upadhyay RS, Gomes EV, Tsui CKM, Nayak SC (2015) Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev 40:182–207

    Google Scholar 

  • Zhang Y, Zheng LX, Liu XJ, Jickells T, Capec JN, Gouldingd K, Fangmeiere A, Zhang FS (2008) Evidence for organic N deposition and its anthropogenic sources in China. Atmos Environ 42:1035–1041

    CAS  Google Scholar 

  • Zhang HF, Wang LL, Liu HM, Zhao JN, Li G, Wang H, Lai X, Li J, Xiu WM, Yang DL (2018) Nitrogen deposition combined with elevated precipitation is conducive to maintaining the stability of the soil fungal diversity on the Stipa baicalensis steppe. Soil Biol Biochem 117:135–138

    CAS  Google Scholar 

  • Zhou J, Jiang X, Zhou BK, Zhao BS, Ma MC, Guan DW, Li J, Chen SF, Cao FM, Shen DL, Qin J (2016) Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol Biochem 95:135–143

  • Zhou JZ, Deng Y, Luo F, He ZL, Tu QC, Zhi XY (2010) Functional molecular ecological networks. MBio 1: e169.

  • Zhou JZ, Deng Y, Luo F, He ZL, Yang YF (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. MBio 2: e00122.

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Funding

This research was financially supported by The Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0308), the National Key Research and Development Program of China (2016YFC0500702) and the National Natural Science Foundation of China (41877046 and 41501265).

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Correspondence to Yongliang Chen.

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Responsible editor: Jizheng He

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Chen, Y., Xu, Z., Feng, K. et al. Nitrogen and water addition regulate soil fungal diversity and co-occurrence networks. J Soils Sediments 20, 3192–3203 (2020). https://doi.org/10.1007/s11368-020-02629-9

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