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

  • Lie Xiao
  • Guobin Liu
  • Peng Li
  • Sha XueEmail author
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article

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.

Keywords

Elevated CO2 Nitrogen deposition Phospholipid fatty acids Soil–microbe–plant system Structural equation modeling 

Notes

Acknowledgements

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

Funding information

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).

References

  1. Bao SD (2000) Soil and agricultural chemistry analysis, 3rd edn. China Agriculture Press, Beijing, pp 268–270Google Scholar
  2. 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 80:3103–3112CrossRefGoogle Scholar
  3. 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 14:1025–1036CrossRefGoogle Scholar
  4. Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831–841CrossRefGoogle Scholar
  5. 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 6:130CrossRefGoogle Scholar
  6. 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 61:65–73CrossRefGoogle Scholar
  7. 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 44:667–679CrossRefGoogle Scholar
  8. 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 18:435–447CrossRefGoogle Scholar
  9. 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 316:311–322CrossRefGoogle Scholar
  10. 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 16:2104–2116CrossRefGoogle Scholar
  11. 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 70:153–226CrossRefGoogle Scholar
  12. 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 170:331–336CrossRefGoogle Scholar
  13. 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 57:390–400CrossRefGoogle Scholar
  14. 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 60:1–9CrossRefGoogle Scholar
  15. 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 168:113–120CrossRefGoogle Scholar
  16. 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 215:1373–1384CrossRefGoogle Scholar
  17. 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:e0120190CrossRefGoogle Scholar
  18. 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 134:845–856CrossRefGoogle Scholar
  19. 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 38:991–999CrossRefGoogle Scholar
  20. 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 120:48–57CrossRefGoogle Scholar
  21. 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 99:5295–5305CrossRefGoogle Scholar
  22. 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 117:129–136CrossRefGoogle Scholar
  23. 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 236:1205–1213CrossRefGoogle Scholar
  24. 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:e112609CrossRefGoogle Scholar
  25. 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 292:25–33CrossRefGoogle Scholar
  26. 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 10:730–738CrossRefGoogle Scholar
  27. 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 5:376–390CrossRefGoogle Scholar
  28. 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 19:208–216CrossRefGoogle Scholar
  29. 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 494:459–462CrossRefGoogle Scholar
  30. 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:e0172382CrossRefGoogle Scholar
  31. Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Glob Chang Biol 24:1–12CrossRefGoogle Scholar
  32. 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 14:187–194CrossRefGoogle Scholar
  33. 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 73:377–395CrossRefGoogle Scholar
  34. Ramirez KS, Craine JM, Fierer N (2010) Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied. Soil Biol Biochem 42:2336–2338CrossRefGoogle Scholar
  35. 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:e03R01CrossRefGoogle Scholar
  36. 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 14:33–47CrossRefGoogle Scholar
  37. 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 14:1861–1868CrossRefGoogle Scholar
  38. 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 42:968–977CrossRefGoogle Scholar
  39. 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 9:2247–2258CrossRefGoogle Scholar
  40. 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 70:809–818CrossRefGoogle Scholar
  41. 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:fnx077CrossRefGoogle Scholar
  42. Toberman H, Chen CR, Xu ZH (2011) Rhizosphere effects on soil nutrient dynamics and microbial activity in an Australian tropical lowland rainforest. Soil Res 49:652–660CrossRefGoogle Scholar
  43. 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:e66563CrossRefGoogle Scholar
  44. 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 415:423–434CrossRefGoogle Scholar
  45. 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 4:78CrossRefGoogle Scholar
  46. 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 19:3699–3697CrossRefGoogle Scholar
  47. 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 83:325–334CrossRefGoogle Scholar
  48. 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 7:6527CrossRefGoogle Scholar
  49. 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 101:72–83CrossRefGoogle Scholar
  50. 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 20:2230–2239CrossRefGoogle Scholar
  51. 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 23:2450–2463CrossRefGoogle Scholar
  52. 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 92:41–49CrossRefGoogle Scholar
  53. 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 29:1837–1849CrossRefGoogle Scholar
  54. 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 385:189–197CrossRefGoogle Scholar
  55. 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 57:888–896CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Eco-hydraulics in Northwest Arid Region of ChinaXi’an University of TechnologyXi’anPeople’s Republic of China
  2. 2.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water ConservationNorthwest A&F UniversityYanglingPeople’s Republic of China
  3. 3.Institute of Soil and Water ConservationChinese Academy of Sciences and Ministry of Water ResourcesYanglingPeople’s Republic of China

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