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Nitrogen competition between three dominant plant species and microbes in a temperate grassland

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Abstract

Background and aims

To test the hypothesis that dominant plant species could acquire different nitrogen (N) forms over a spatial scale and they also have the ability to compete for available N with microbes.

Methods

A short-term 15N labeling experiment was conducted in the temperate grassland ecosystem of North China in July of 2013. Three N forms (NO3 , NH4 + and glycine) labeled with 15N were injected into the two soil depths (0–5 and 5–15 cm) surrounding each plant to explore N acquisition by plants and microbes. Three dominant plant species (Artemisia frigida, Cleistogenes squarrosa and Artemisia capillaris) were investigated.

Results

Two hours after 15N labeling, all three dominant plant species absorbed both organic and inorganic N, but different patterns were observed at two soil depths. Uptake of NO3 was significantly higher at 0–5 cm than at 5–15 cm soil depth among all the dominant plant species. 15N recovery by microbes was significantly higher than plants. However, 15N recovery by plants showed different patterns over soil depths.

Conclusions

Dominant plant species in the temperate grassland have different patterns in acquisition of N added to soil in organic form and absorption of inorganic N, and microbes were more effectively than plants at competing for N in a short-term period.

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References

  • Andresen LC, Jonasson S, Ström L, Michelsen A (2008) Uptake of pulse injected nitrogen by soil microbes and mycorrhizal and non-mycorrhizal plants in a species-diverse subarctic heath ecosystem. Plant Soil 313(1–2):283–295

    Article  CAS  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91(11):3252–3260

    Article  PubMed  Google Scholar 

  • Bardgett RD, Streeter TC, Cole L, Hartley IR (2002) Linkages between soil biota, nitrogen availability, and plant nitrogen uptake in a mountain ecosystem in the Scottish highlands. Appl Soil Ecol 19:121–134

    Article  Google Scholar 

  • Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Buckeridge KM, Jefferies RL (2007) Vegetation loss alters soil nitrogen dynamics in an Arctic salt marsh. J Ecol 95:283–293

    Article  CAS  Google Scholar 

  • Chinese Academy of Science (2001) The Chinese soil taxonomic classification retrieval, 3rd edn. Press of University of Science and Technology of China, Hefei

    Google Scholar 

  • Clemmensen KE, Sorensen PL, Michelsen A, Jonasson S, Ström L (2008) Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155(4):771–783

    Article  PubMed  Google Scholar 

  • Finzi AC, Berthrong ST (2005) The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology 86(12):3345–3353

    Article  Google Scholar 

  • Fischer H, Ingwersen J, Kuzyakov Y (2010) Microbial uptake of low-molecular-weight organic substances out-competes sorption in soil. Eur J Soil Sci 61:504–513

    Article  CAS  Google Scholar 

  • Gao JQ, Mo Y, Xu XL, Zhang XW, Yu FH (2014) Spatiotemporal variations affect uptake of inorganic and organic nitrogen by dominant plant species in an alpine wetland. Plant Soil 381:271–278

    Article  CAS  Google Scholar 

  • Gioseffi E, de Neergaard A, Schjoerring JK (2012) Interactions between uptake of amino acids and inorganic nitrogen in wheat plants. Biogeosciences 9(4):1509–1518

    Article  CAS  Google Scholar 

  • Harrison KA, Roland B, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999

    Article  PubMed  Google Scholar 

  • Harrison KA, Bol R, Bardgett RD (2008) Do plant species with different growth strategies vary in their ability to compete with soil microbes for chemical forms of nitrogen? Soil Biol Biochem 40:228–237

    Article  CAS  Google Scholar 

  • Hertenberger G, Wanek W (2004) Evaluation of methods to measure differential 15 N labeling of soil and root N pools for studies of root exudation. Rapid Commun Mass Spectrom 18(20):2415–2425

    Article  CAS  PubMed  Google Scholar 

  • Hill PW, Farrar J, Roberts P, Farrell M, Grant H, Newsham KK, Hopkins DW, Bardgett RD, Jones DL (2011a) Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition. Nat Clim Chang 1(1):50–53

    Article  CAS  Google Scholar 

  • Hill PW, Quilliam RS, DeLuca TH, Farrar J, Farrell M, Roberts P, Newsham KK, Hopkins DW, Bardgett RD, Jones DL (2011b) Acquisition and assimilation of nitrogen as peptide-bound and denantiomers of amino acids by wheat. PLoS One 6(4):e19220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill PW, Farrell M, Jones DL (2012) Bigger may be better in soil N cycling: does rapid acquisition of small l-peptides by soil microbes dominate fluxes of protein-derived N in soil? Soil Biol Biochem 48:106–112

    Article  CAS  Google Scholar 

  • Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J Ecol 88:150–164

    Article  Google Scholar 

  • Huang WY, Cai YZ, Surveswaran S, Hyde KD, Corke H, Sun M (2009) Molecular phylogenetic identification of endophytic fungi isolated from three Artemisia species. Fungal Divers 36:69–88

    CAS  Google Scholar 

  • Jackson LE, Schimel JP, Firestone MK (1989) Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland. Soil Biol Biochem 21:409–415

    Article  Google Scholar 

  • Jaeger CH, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology 80:1883–1891

    Article  Google Scholar 

  • Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219

    Article  CAS  Google Scholar 

  • Kalembasa SJ, Jenkinson DS (1973) A comparative study of titrimetric and gravimetric methods for the determination of organic carbon in soil. J Sci Food Agric 24:1085–1090

    Article  CAS  Google Scholar 

  • Kaštovská E, Šantrůčková H (2011) Comparison of uptake of different N forms by soil microorganisms and two wet-grassland plants: a pot study. Soil Biol Biochem 43:1285–1291

    Article  Google Scholar 

  • Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12(4):139–143

    Article  CAS  PubMed  Google Scholar 

  • Kleinebecker T, Hölzel N, Prati D, Schmitt B, Fischer M, Klaus VH (2014) Evidence from the real world: 15N natural abundances reveal enhanced nitrogen use at high plant diversity in central European grasslands. J Ecol 102:456–465

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Xu XL (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669

    Article  CAS  PubMed  Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115

    Article  CAS  Google Scholar 

  • Lebauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystem is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  • Marion GM, Miller PC, Kummerow J, Oechel WC (1982) Competition for nitrogen in a tussock tundra ecosystem. Plant Soil 66:317–327

    Article  CAS  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JL, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    Article  CAS  PubMed  Google Scholar 

  • Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292

    Article  CAS  Google Scholar 

  • Miller AJ, Cramer MD (2005) Root physiology from gene to function. In: Lambers H, Colmer TD (eds) Root nitrogen acquisition and assimilation, vol 4. Springer, Netherlands, pp. 1–36

    Google Scholar 

  • Miller AE, Bowman WD, Suding KN (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88(7):1832–1840

  • Näsholm T, Sandberg G, Ericsson A (1987) Quantitative analysis of amino acids in conifer tissues by high-performance liquid chromatography and fluorescence detection of their 9-fluorenylmethyl chloroformate derivatives. J Chromatogr A 396:225–236

    Article  Google Scholar 

  • Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48

    Article  PubMed  Google Scholar 

  • Nye PH, Tinker PB (1977) Solute movement in the soil-root systems. University of California Press, Berkeley

    Google Scholar 

  • Oses R, Valenzuela S, Freer J, Sanfuentes E, Rodríguez J (2008) Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Divers 33:77–86

    Google Scholar 

  • Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem 33:651–657

    Article  CAS  Google Scholar 

  • Paungfoo-Lonhienne C, Lonhienne TG, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. Proc Natl Acad Sci U S A 105(11):4524–4529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paungfoo-Lonhienne C, Visser J, Lonhienne TGA, Schmidt S (2012) Past, present and future of organic nutrients. Plant Soil 359(1–2):1–18

    Article  CAS  Google Scholar 

  • Pruden G, Powlson DS, Jenkinson DS (1985) The measurement of 15N in soil and plant material. Fert Res 6(3):205–218

    Article  CAS  Google Scholar 

  • Raab TK, Lipson DA, Monson RK (1996) Non-mycorrhizal uptake of amino acids by roots of the alpine sedge Kobresia myosuroides: implications for the alpine nitrogen cycle. Oecologia 108:488–494

  • Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the cyperaceae: plant and soil processes. Ecology 80:2408–2419

    Article  Google Scholar 

  • Rosswall T (1982) Microbiological regulation of the biogeochemical nitrogen cycle. Plant Soil 67:15–34

    Article  CAS  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Schimel JP, Chapin FS (1996) Tundra plant uptake of amino acid and NH4 + nitrogen in situ: plants complete well for amino acid N. Ecology 77:2142–2147

    Article  Google Scholar 

  • Soil Survey Staff (1987) Keys to soil taxonomy, 3rd edn. Cornell University, New York

    Google Scholar 

  • Song MH, Xu XL, Hu QW, Tian YQ, Ouyang H, Zhou CP (2007) Interactions of plant species mediated plant competition for inorganic nitrogen with soil microorganisms in an alpine meadow. Plant Soil 297:127–137

    Article  CAS  Google Scholar 

  • Sorensen PL, Michelsen A, Jonasson S (2008) Ecosystem partitioning of 15N-glycine after long-term climate and nutrient manipulations, plant clipping and addition of labile carbon in a subarctic heath tundra. Soil Biol Biochem 40:2344–2350

    Article  CAS  Google Scholar 

  • Vitousek P, Howarth R (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Wang WY, Ma YG, Xu J, Wang HC, Zhu JF, Zhou HK (2012) The uptake diversity of soil nitrogen nutrients by main plant species in Kobresia humilis alpine meadow on the Qinghai-Tibet plateau. Sci China Earth Sci 55:1688–1695

    Article  CAS  Google Scholar 

  • Weigelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635

    Article  PubMed  Google Scholar 

  • Werth M, Kuzyakov Y (2010) 13C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42(9):1372–1384

    Article  CAS  Google Scholar 

  • Wilkinson A, Hill PW, Farrar JF, Jones DL, Bardgett RD (2014) Rapid microbial uptake and mineralization of amino acids and peptides along a grassland productivity gradient. Soil Biol Biochem 72:75–83

    Article  CAS  Google Scholar 

  • Wilkinson A, Hill PW, Vaieretti MV, Farrar JF, Jones DL, Bardgett RD (2015) Challenging the paradigm of nitrogen cycling: no evidence of in situ resource partitioning by coexisting plant species in grasslands of contrasting fertility. Ecol Evol 5(2):275–287

    Article  PubMed  Google Scholar 

  • Wu HH, Dannenmann M, Fanselow N, Wolf B, Yao ZS, Wu X, Brüggemann N, Zheng XH, Han XG, Dittert K, Butterbach-Bahl K (2011) Feedback of grazing on gross rates of N mineralization and inorganic N partitioning in steppe soils of inner Mongolia. Plant Soil 340:127–139

    Article  CAS  Google Scholar 

  • Wu JR, Ma HC, Xu XL, Qiao N (2013) Mycorrhizas alter nitrogen acquisition pattern of a soil dwelling orchid (Cymbidium goeringii): evidence from a short-term 15N experiment. Ann Bot 111:1181–1187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu L, Gao Q, Wang YL (2014) Species richness within a six-year slope exclosure in a temperate grassland and its relationship with aboveground biomass. Ecol Environ Sci 23(3):398–405

    Google Scholar 

  • Xu XL, Ouyang H, Kuzyakov Y, Richter A, Wanek W (2006) Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant Soil 285(1-2):221–231

  • Xu XL, Ouyang H, Cao GM, Richter A, Wanek W, Kuzyakov Y (2011a) Dominant plant species shift their nitrogen uptake patterns in response to nutrient enrichment caused by a fungal fairy in an alpine meadow. Plant Soil 341:495–504

    Article  CAS  Google Scholar 

  • Xu XL, Ouyang H, Richter A, Wanek W, Cao GM, Kuzyakov Y (2011b) Spatio-temporal variations determine plant-microbe competition for inorganic nitrogen in an alpine meadow. J Ecol 99:563–571

    CAS  Google Scholar 

  • Zhan BL, Chen SH, Zhang H, Cao LX, Buren JY (1999) A research of characteristics and ecological distribution of Artemisia frigida. J Inn Mongolia Inst Agric Anim Husb 20:1–7

    CAS  Google Scholar 

  • Zhang YH, He NP, Zhang GM, Huang JH, Wang QB, Pan QM, Han XG (2013) Ammonia emissions from soil under sheep grazing in inner Mongolian grasslands of China. J Arid Land 5:155–165

    Article  Google Scholar 

  • Zhu WX, Carreiro MM (2004) Temporal and spatial variations in nitrogen transformations in deciduous forest ecosystems along an urban rural gradient. Soil Biol Biochem 36:267–278

    Article  CAS  Google Scholar 

  • Zogg GP, Zak DR, Pregitzer KS, Burton AJ (2000) Microbial immobilization and the retention of anthropogenic nitrate in a northern hardwood forest. Ecology 81:1858–1866

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the “National Key Basic Research Program of China” (Grant No. 2014CB138803), the Fundamental Research Funds for Central Universities (Grant No. 2014KJJCB01) and the State Key Laboratory of Earth Surface Processes and Resource Ecology, Beijing Normal University (Grant No. 2009-RC-03) as well as National Natural Science Foundation of China (31470560, 41071209 and 31570468).

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Correspondence to Yuqiang Tian.

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Responsible Editor: Ad C. Borstlap.

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Ouyang, S., Tian, Y., Liu, Q. et al. Nitrogen competition between three dominant plant species and microbes in a temperate grassland. Plant Soil 408, 121–132 (2016). https://doi.org/10.1007/s11104-016-2904-3

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