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Direct and indirect effects of elevated CO2 and nitrogen addition on soil microbial communities in the rhizosphere of Bothriochloa ischaemum

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
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Abstract

Purpose

Elevated CO2 and nitrogen (N) addition both affect soil microbial communities, which significantly influence soil processes and plant growth. Here, we evaluated the combined effects of elevated CO2 and N addition on the soil–microbe–plant system of the Chinese Loess Plateau.

Materials and methods

A pot cultivation experiment with two CO2 treatment levels (400 and 800 μmol mol−1) and three N addition levels (0, 2.5, and 5 g N m−2 year−1) was conducted in climate-controlled chambers to evaluate the effects of elevated CO2 and N addition on microbial community structure in the rhizosphere of Bothriochloa ischaemum using phospholipid fatty acid (PLFA) profiles and associated soil and plant properties. Structural equation modeling (SEM) was used to identify the direct and indirect effects of the experimental treatments on the structure of microbial communities.

Results and discussion

Elevated CO2 and N addition both increased total and fungal PLFAs. N addition alone increased bacterial, Gram-positive, and Gram-negative PLFAs. However, elevated CO2 interacting with N addition had no significant effects on the microbial community. The SEM indicated that N addition directly affected the soil microbial community structure. Elevated CO2 and N addition both indirectly affected the microbial communities by affecting plant and soil variables. N addition exerted a stronger total effect than elevated CO2.

Conclusions

The results highlighted the importance of comprehensively studying soil–microbe–plant systems to deeply reveal how characteristics of terrestrial ecosystems may respond under global change.

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References

  • Bao SD (2000) Soil and agricultural chemistry analysis, 3rd edn. China Agriculture Press, Beijing, pp 268–270

    Google Scholar 

  • Berthrong ST, Yeager CM, Gallegos-Graves L (2014) Nitrogen fertilization has a stronger effect on soil nitrogen-fixing bacterial communities than elevated atmospheric CO2. Appl Environ Microbiol 80:3103–3112

    Google Scholar 

  • Billings SA, Ziegler SE (2008) Altered patterns of soil carbon substrate usage and heterotrophic respiration in a pine forest with elevated CO2 and N fertilization. Glob Chang Biol 14:1025–1036

    Google Scholar 

  • Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831–841

    CAS  Google Scholar 

  • Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CM (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: what lies ahead? Ecosphere 6:130

    Google Scholar 

  • Deng Q, Cheng XL, Zhou GY, Liu JX, Liu SZ, Zhang QF, Zhang DQ (2013) Seasonal responses of soil respiration to elevated CO2 and N addition in young subtropical forest ecosystems in southern China. Ecol Eng 61:65–73

    Google Scholar 

  • Drigo B, Kowalchuk CA, van Veen JA (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679

    Google Scholar 

  • Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB (2012) Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Chang Biol 18:435–447

    Google Scholar 

  • Esmeijer-Liu AJ, Aerts R, Kurschner WM, Bobbink R, Lotter AF, Cerhoeven JTA (2009) Nitrogen enrichment lowers Betula pendula green and yellow leaf stoichiometry irrespective of effects of elevated carbon dioxide. Plant Soil 316:311–322

    CAS  Google Scholar 

  • Feng XJ, Simpson AJ, Schlesinger WH, Simpson MJ (2010) Altered microbial community structure and organic matter composition under elevated CO2 and N fertilization in the duke forest. Glob Chang Biol 16:2104–2116

    Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vörösmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    CAS  Google Scholar 

  • Guenet B, Lenhart K, Leloup J, Giusti-Miller S, Pouteau V, Mora P, Nunan N, Abbadie L (2012) The impact of long-term CO2 enrichment and moisture levels on soil microbial community structure and enzyme activities. Geoderma 170:331–336

    CAS  Google Scholar 

  • Hagedorn F, Hiltbrunner D, Streit K, Ekblad A, Lindahl B, Miltner A, Frey B, Handa IT, Hattenschwiler S (2013) Nine years of CO2 enrichment at the alpine treeline stimulates soil respiration but does not alter soil microbial communities. Soil Biol Biochem 57:390–400

    CAS  Google Scholar 

  • Han XW, Tsunekawa A, Tsubo M, Shao HB (2013) Responses of plant-soil properties to increasing N deposition and implications for large-scale eco-restoration in the semiarid grassland of the northern Loess Plateau, China. Ecol Eng 60:1–9

    Google Scholar 

  • Huang WJ, Zhou GY, Liu JX, Zhang DQ, Xu ZH, Liu SZ (2012) Effects of elevated carbon dioxide and nitrogen addition on foliar stoichiometry of nitrogen and phosphorus of five tree species in subtropical model forest ecosystems. Environ Pollut 168:113–120

    CAS  Google Scholar 

  • Huang WJ, Zhou GY, Liu JX, Duan HL, Liu XZ, Fang X, Zhang DQ (2014) Shifts in soil phosphorus fractions under elevated CO2 and N addition in model forest ecosystems in subtropical China. Plant Ecol 215:1373–1384

    Google Scholar 

  • Huang WJ, Zhou GY, Liu JX, Zhang DQ, Liu SZ, Chu GW, Fang X (2015a) Mineral elements of subtropical tree seedlings in response to elevated carbon dioxide and nitrogen addition. PLoS One 10:e0120190

    Google Scholar 

  • Huang WJ, Zhou GY, Deng XF, Liu JX, Duan HL, Zhang DQ, Chu GW, Liu SZ (2015b) Nitrogen and phosphorus productivities of five subtropical tree species in response to elevated CO2 and N addition. Eur J For Res 134:845–856

    CAS  Google Scholar 

  • Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999

    CAS  Google Scholar 

  • Koyama A, Harlow B, Kuske CR, Belnap J, Evans RD (2018) Plant and microbial biomarkers suggest mechanisms of soil organic carbon accumulation in a Mojave Desert ecosystem under elevated CO2. Soil Biol Biochem 120:48–57

    CAS  Google Scholar 

  • Lee SH, Kim SY, Ding WX, Kang H (2015) Impact of elevated CO2 and N addition on bacteria, fungi, and archaea in a marsh ecosystem with various types of plants. Appl Microbiol Biotechnol 99:5295–5305

    CAS  Google Scholar 

  • Lee SH, Megonigal PJ, Langley AJ, Kang H (2017) Elevated CO2 and nitrogen addition affect the microbial abundance but not the community structure in salt marsh ecosystem. Appl Soil Ecol 117:129–136

    Google Scholar 

  • Lei YB, Wang WB, Feng YL, Zheng YL, Gong HD (2012) Synergistic interactions of CO2 enrichment and nitrogen deposition promote growth and ecophysiological advantages of invading Eupatorium adenophorum in Southwest China. Planta 236:1205–1213

    CAS  Google Scholar 

  • Li XZ, Rui JP, Xiong JB, Li JB, He ZL, Zhou JZ, Yannarell AC, Mackie RI (2014) Functional potential of soil microbial communities in the maize rhizosphere. PLoS One 9:e112609

    Google Scholar 

  • Ling N, Chen DM, Guo H, Wei JX, Bai YF, Shen QR, Hu SJ (2017) Differential responses of soil bacterial communities to long-term N and P inputs in a semi-arid steppe. Geoderma 292:25–33

    CAS  Google Scholar 

  • Liu JX, Zhou GY, Zhang DQ, Xu ZH, Duan HL, Deng Q, Zhao L (2010) Carbon dynamics in subtropical forest soil: effects of atmospheric carbon dioxide enrichment and nitrogen addition. J Soils Sediments 10:730–738

    CAS  Google Scholar 

  • Liu JX, Zhang DQ, Zhou GY, Duan HL (2012) Changes in leaf nutrient traits and photosynthesis of four tree species: effects of elevated CO2, N fertilization and canopy positions. J Plant Ecol 5:376–390

    Google Scholar 

  • Liu JX, Huang WJ, Zhou GY, Zhang DQ, Liu SZ, Li YY (2013a) Nitrogen to phosphorus ratios of tree species in response to elevated carbon dioxide and nitrogen addition in subtropical forests. Glob Chang Biol 19:208–216

    Google Scholar 

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

    CAS  Google Scholar 

  • Lv FL, Xue S, Wang GL, Zhao C (2017) Nitrogen addition shifts the microbial community in the rhizosphere of Pinus tabuliformis in Northwestern China. PLoS One 12:e0172382

    Google Scholar 

  • Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Glob Chang Biol 24:1–12

    Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194

    Google Scholar 

  • Porazinska DL, Bardgett RD, Blaauw MB, Willliam Hunt H, Parsons AN, Seastedt TR, Wall DH (2003) Relationships at the aboveground–belowground interface: plants, soil biota, and soil processes. Ecol Monogr 73:377–395

    Google Scholar 

  • Ramirez KS, Craine JM, Fierer N (2010) Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied. Soil Biol Biochem 42:2336–2338

    CAS  Google Scholar 

  • Santoyo G, Hermandez-Pacheco C, Hernandez-Salmeron J, Hernandez-Leon R (2017) The role of abiotic factors modulating the plant-microbe-soil interactions: toward sustainable agriculture. A review. Span J Agric Res 15:e03R01

    Google Scholar 

  • Sardans J, Rivas-Ubach A, Penuelas J (2012) The C:N:P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspect Plant Ecol 14:33–47

    Google Scholar 

  • Shen JP, Zhang LM, He JZ (2014) Contrasting response of nitrification capacity in three agricultural soils to N addition during short-term incubation. J Soils Sediments 14:1861–1868

    CAS  Google Scholar 

  • Siegenthaler A, Buttler A, Bragazza L, van der Heijiden E, Grosvernier P, Gobat JM, Mitchell EAD (2010) Litter- and ecosystem-driven decomposition under elevated CO2 and enhanced N deposition in a Sphagnum peatland. Soil Biol Biochem 42:968–977

    CAS  Google Scholar 

  • Sillen WMA, Dieleman WIJ (2012) Effects of elevated CO2 and N fertilization on plant and soil carbon pools of managed grasslands: a meta-analysis. Biogeosciences 9:2247–2258

    CAS  Google Scholar 

  • Simonin M, Le Roux X, Poly F, Lerondelle C, Hungate BA, Nunan N, Niboyet A (2015) Coupling between and among ammonia oxidizers and nitrite oxidizers in grassland mesocosms submitted to elevated CO2 and nitrogen supply. Microb Ecol 70:809–818

    CAS  Google Scholar 

  • Simonin M, Nunan N, Bloor JMG, Pouteau V, Niboyet A (2017) Short-term responses and resistance of soil microbial community structure to elevated CO2 and N addition in grassland mesocosms. FEMS Microbiol Lett 364:fnx077

    Google Scholar 

  • Toberman H, Chen CR, Xu ZH (2011) Rhizosphere effects on soil nutrient dynamics and microbial activity in an Australian tropical lowland rainforest. Soil Res 49:652–660

    CAS  Google Scholar 

  • Wang JB, Zhu TC, Ni HW, Zhong HX, Fu XL, Wang JF (2013) Effects of elevated CO2 and nitrogen deposition on ecosystem carbon fluxes on the Sanjiang Plain wetland in Northeast China. PLoS One 8:e66563

    CAS  Google Scholar 

  • Wang GL, Xue S, Liu F, Liu GB (2017) Nitrogen addition increases the production and turnover of the lower-order roots but not of the higher-order roots of Bothriochloa ischaemum. Plant Soil 415:423–434

    CAS  Google Scholar 

  • Weber CF, Vilgalys R, Kuske CR (2013) Changes in fungal community composition in response to elevated atmospheric CO2 and nitrogen fertilization varies with soil horizon. Front Microbiol 4:78

    CAS  Google Scholar 

  • Wei CZ, Yu Q, Bai E, Lu XT, Li Q, Xia JY, Kardol P, Liang WJ, Wang ZW, Han XG (2013) Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems. Glob Chang Biol 19:3699–3697

    Google Scholar 

  • Xiao L, Liu GB, Li P, Xue S (2017a) Nitrogen addition has a stronger effect on stoichiometries of non-structural carbohydrates, nitrogen and phosphorus in Bothriochloa ischaemum than elevated CO2. Plant Growth Regul 83:325–334

    CAS  Google Scholar 

  • Xiao L, Liu GB, Li P, Xue S (2017b) Elevated CO2 and nitrogen addition have minimal influence on the rhizospheric effects of Bothriochloa ischaemum. Sci Rep 7:6527

    Google Scholar 

  • Xiong QL, Pan KW, Zhang L, Wang YJ, Li W, He XJ, Luo HY (2016) Warming and nitrogen deposition are interactive in shaping surface soil microbial communities near the alpine timberline zone on the eastern Qinghai-Tibet Plateau, southwestern China. Appl Soil Ecol 101:72–83

    Google Scholar 

  • Yan JH, Zhang DQ, Liu JX, Zhou GY (2014) Interactions between CO2 enhancement and N addition on net primary productivity and water-use efficiency in a mesocosm with multiple subtropical tree species. Glob Chang Biol 20:2230–2239

    Google Scholar 

  • Yue K, Fornara DA, Yang WQ, Peng Y, Li ZJ, Wu FS, Peng CH (2017) Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis. Glob Chang Biol 23:2450–2463

    Google Scholar 

  • Zeng J, Liu XJ, Song L, Lin XG, Zhang HY, Shen CC, Chu HY (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49

    CAS  Google Scholar 

  • Zhang T, Cao Y, Chen YM, Liu GB (2015) Non-structural carbohydrate dynamics in Robinia pseudoacacia saplings under three levels of continuous drought stress. Trees 29:1837–1849

    CAS  Google Scholar 

  • Zhang L, Zou JW, Siemann E (2017) Interactive effects of elevated CO2 and nitrogen deposition accelerate litter decomposition cycles of invasive tree (Triadica sebifera). For Ecol Manag 385:189–197

    Google Scholar 

  • Zhu YG, Duan GL, Chen BD, Peng XH, Chen Z, Sun GX (2014) Mineral weathering and element cycling in soil-microorganism-plant system. Sci China Earth Sci 57:888–896

    CAS  Google Scholar 

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Acknowledgements

We would like to thank Prof. Simon Queenborough at the Yale University for his assistance with English language editing of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (41701603), Program for Science & Technology Innovation Research Team of Shaanxi Province (2018TD-037), and Western Young Scholars Project of the Chinese Academy of Sciences (XAB2015A05).

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Correspondence to Sha Xue.

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Responsible editor: Yongfu Li

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Xiao, L., Liu, G., Li, P. et al. Direct and indirect effects of elevated CO2 and nitrogen addition on soil microbial communities in the rhizosphere of Bothriochloa ischaemum. J Soils Sediments 19, 3679–3687 (2019). https://doi.org/10.1007/s11368-019-02336-0

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