Skip to main content
Log in

Nitrogen addition shapes soil enzyme activity patterns by changing pH rather than the composition of the plant and microbial communities in an alpine meadow soil

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Increasing nitrogen (N) deposition has considerable effects on soil organic matter (SOM) decomposition mediated by soil enzyme activities. Few studies, however, have explored how N addition shapes soil enzyme activity patterns by changing plants, soils and microbes.

Methods

We conducted a five-year field fertilization experiment (0, 5, 10, and 15 g N m−2 yr.−1) to study how N addition affected soil enzyme activity patterns in the topsoil (0–20 cm) and subsoil (20–40 cm) in a Tibetan alpine meadow. Enzyme activity patterns were calculated by the percentage of the sum of all measured enzyme activities. The composition of the plant and microbial communities were evaluated through measuring the abundance of plant functional groups and quantifying microbial phospholipid fatty acids (PLFAs), respectively. Soil pH and available N were also measured.

Results

We found that soil N availability primarily controlled plant community composition, but pH controlled the composition of the microbial community, irrespective of soil depth. Soil enzyme activity patterns differed between two soil depths and among N addition rates. Importantly, N addition shaped soil enzyme activity patterns through the changes in soil pH rather than via the composition of the plant and microbial communities.

Conclusions

Our findings indicate that N addition can affect components of plant-soil system and, in particular, weaken the linkages between plant and microbial communities and enzyme activity patterns. The work suggests that N enrichment-induced soil acidification plays a key role in SOM decomposition and nutrient cycling in the Tibetan meadow ecosystem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

C:

Carbon

N:

Nitrogen

P:

Phosphorus

SOM:

Soil organic matter

SEM:

Structural equation model

PLFAs:

Phospholipid fatty acids

Control:

0 g N m−2 yr.−1

N5:

5g N m−2 yr.−1

N10:

10 g N m−2 yr.−1

N15:

15 g N m−2 yr.−1

G+:G ratio:

Gram-positive bacteria:gram-negative bacteria

F:B:

Fungi:bacteria

NMDS:

Nonmetric multidimensional scaling

PERMANOVA:

Permutational multivariate analysis of variance

PCA:

Principal component analysis

BG:

β-1,4-glucosidase

UREA:

Urease

AP:

Acid phosphomonoesterase

PHO:

Phenol oxidase

References

  • Allison VJ, Condron LM, Peltzer DA, Richardson SJ, Turner BL (2007) Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol Biochem 39:1770–1781

    Article  CAS  Google Scholar 

  • Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Shukla G, Varma A (eds) Soil enzymology, 1st edn. Springer, Berlin, pp 229–243

    Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han X (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia grasslands. Global Chang Biol 16:358–372

    Article  Google Scholar 

  • Bassin S, Volk M, Suter M, Buchmann N, Fuhrer J (2007) Nitrogen deposition but not ozone affects productivity and community composition of subalpine grassland after 3 yr of treatment. New Phytol 175:523–534

    Article  CAS  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2018) lme4: linear mixed-effects models using ‘Eigen’ and S4. R package version 1:1–17 http://cran.r-project.org/package=lme4. Accessed 3 Apr 2018

    Google Scholar 

  • Bending GD, Turner MK, Jones JE (2002) Interactions between crop residue and soil organic matter quality and the functional diversity of soil microbial communities. Soil Biol Biochem 34:1073–1082

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE (2014) Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol Biochem 68:252–262

    Article  CAS  Google Scholar 

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234

    Article  CAS  Google Scholar 

  • Canarini A, Carrillo Y, Mariotte P, Ingram L, Dijkstra FA (2016) Soil microbial community resistance to drought and links to C stabilization in an Australian grassland. Soil Biol Biochem 103:171–180

    Article  CAS  Google Scholar 

  • Cao GM, Zhang JX (2001) Soil nutrition and substance cycle of Kobresia meadow. In: Zhou XM (ed) Alpine Kobresia meadows in China. Science, Beijing, pp 58–147

    Google Scholar 

  • Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365

    Article  Google Scholar 

  • Chen DM, Lan ZC, Bai X, Grace JB, Bai YF (2013) Evidence that acidification-induced declines in plant diversity and productivity are mediated by changes in below-ground communities and soil properties in a semi-arid steppe. J Ecol 101:1322–1334

    Article  CAS  Google Scholar 

  • Chen DM, Lan ZC, Hu SJH, 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

    Article  CAS  Google Scholar 

  • Davidson EA, Samanta S, Caramori SS, Savage K (2012) The dual Arrhenius and Michaelis-Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Global Chang Biol 18:371–384

    Article  Google Scholar 

  • Delgado-Baquerizo M, Grinyer J, Reich PB, Singh BK (2016) Relative importance of soil properties and microbial community for soil functionality: insights from a microbial swap experiment. Funct Ecol 30:1862–1873

    Article  Google Scholar 

  • Dunn RM, Mikola J, Bol R, Bardgett RD (2006) Influence of microbial activity on plant-microbial competition for organic and inorganic nitrogen. Plant Soil 289:321–334

    Article  CAS  Google Scholar 

  • Eskelinen A, Stark S, Mannisto M (2009) Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats. Oecologia 161:113–123

    Article  PubMed  Google Scholar 

  • Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176

    Article  CAS  Google Scholar 

  • Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–462

    Article  Google Scholar 

  • Frossard A, Gerull L, Mutz M, Gessner MO (2012) Disconnect of microbial structure and function: enzyme activities and bacterial communities in nascent stream corridors. ISME J 6:680–691

    Article  CAS  PubMed  Google Scholar 

  • Frostegåd A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  • Frostegård Å, Bååth E, Tunlio A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730

    Article  Google Scholar 

  • Ge T, Wei X, Razavi BS, Zhu Z, Hu Y, Kuzyakov Y, Jones DL, Wu J (2017) Stability and dynamics of enzyme activity patterns in the rice rhizosphere: effects of plant growth and temperature. Soil Biol Biochem 113:108–115

    Article  CAS  Google Scholar 

  • Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms – a review. Soil Biol Biochem 75:54–63

    Article  CAS  Google Scholar 

  • Heitkötter J, Niebuhr J, Heinze S, Marschner B (2017) Patterns of nitrogen and citric acid induced changes in C-turnover and enzyme activities are different in topsoil and subsoils of a sandy Cambisol. Geoderma 292:111–117

    Article  CAS  Google Scholar 

  • Hernández DL, Hobbie SE (2010) The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil 335:397–411

    Article  CAS  Google Scholar 

  • Hu YJ, Xiang D, Veresoglou SD, Chen FL, Chen YL, Hao ZP, Zhang X, Chen BD (2014) Soil organic carbon and soil structure are driving microbial abundance and community composition across the arid and semi-arid grasslands in northern China. Soil Biol Biochem 77:51–57

    Article  CAS  Google Scholar 

  • Jackson CR, Liew KC, Yule CM (2009) Structural and functional changes with depth in microbial communities in a tropical Malaysian peat swamp forest. Microb Ecol 57:402–412

    Article  PubMed  Google Scholar 

  • Jia Y, Yu G, He N, Zhan X, Fang H, Sheng W, Zuo Y, Zhang D, Wang Q (2014) Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Sci Rep 4:3763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jian S, Li J, Chen J, Wang G, Mayes MA, Dzantor KE, Hui D, Luo Y (2016) Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis. Soil Biol Biochem 101:32–43

    Article  CAS  Google Scholar 

  • Jing X, Yang X, Ren F, Zhou H, Zhu B, He JS (2016) Neutral effect of nitrogen addition and negative effect of phosphorus addition on topsoil extracellular enzymatic activities in an alpine grassland ecosystem. Appl Soil Ecol 107:205–213

    Article  Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of dmmonium. Biol Fertil Soils 6:68–72

    Article  CAS  Google Scholar 

  • Kjoller R, Nilsson LO, Hansen K, Schmidt IK, Vesterdal L, Gundersen P (2012) Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. New Phytol 194:278–286

    Article  CAS  PubMed  Google Scholar 

  • Lamb EG, Kennedy N, Siciliano SD (2010) Effects of plant species richness and evenness on soil microbial community diversity and function. Plant Soil 338:483–495

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Li X, Zhang X, Wu J, Shen Z, Zhang Y, Xu X, Fan Y, Zhao Y, Yan W (2011) Root biomass distribution in alpine ecosystems of the northern Tibetan plateau. Environ Earth Sci 64:1911–1919

    Article  Google Scholar 

  • Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828

    Article  PubMed  Google Scholar 

  • Manning P, Newington JE, Robson HR et al (2006) Decoupling the direct and indirect effects of nitrogen deposition on ecosystem function. Ecol Lett 9:1015–1024

    Article  PubMed  Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK et al (eds) Phosphorus in action. Springer Verlag, Berlin Heidelberg, pp 215–243

    Chapter  Google Scholar 

  • Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M et al (2018) Vegan:community ecology package. R package version 2:5–2. https://CRAN.R-project.org/package=vegan. Accessed 17 May 2018

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 10 March 2016

  • Riggs CE, Hobbie SE (2016) Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils. Soil Biol Biochem 99:54–65

    Article  CAS  Google Scholar 

  • Rumpel C, Kögel-Knabner I (2011) Deep soil organic matter—a key but poorly understood component of terrestrial C cycle. Plant Soil 338:143–158

    Article  CAS  Google Scholar 

  • Sanaullah M, Blagodatskaya E, Chabbi A, Rumpel C, Kuzyakov Y (2011) Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition. Appl Soil Ecol 48:38–44

    Article  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    Article  CAS  Google Scholar 

  • Schnecker J, Wild B, Hofhansl F et al (2014) Effects of soil organic matter properties and microbial community composition on enzyme activities in cryoturbated arctic soils. PLoS One 9:e94076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnecker J, Wild B, Takriti M et al (2015) Microbial community composition shapes enzyme patterns in topsoil and subsoil horizons along a latitudinal transect in Western Siberia. Soil Biol Biochem 83:106–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi B, Zhang J, Wang C, Ma J, Sun W (2018) Responses of hydrolytic enzyme activities in saline-alkaline soil to mixed inorganic and organic nitrogen addition. Sci Rep 8:4543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Article  PubMed  Google Scholar 

  • Šnajdr J, Valášková V, Merhautová V, Herinková J, Cajthaml T, Baldrian P (2008) Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem 40:2068–2075

    Article  CAS  Google Scholar 

  • Speir TW, Kettles HA, Percival HJ, Parshotam A (1999) Is soil acidifcation the cause of biochemical responses when soils are amended with heavy metal salts? Soil Biol Biochem 31:1953–1961

    Article  CAS  Google Scholar 

  • Stone MM, DeForest JL, Plante AF (2014) Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo critical zone observatory. Soil Biol Biochem 75:237–247

    Article  CAS  Google Scholar 

  • Sun YF, Shen JP, Zhang CJ, Zhang LM, Bai WM, Fang Y, He JZ (2018) Responses of soil microbial community to nitrogen fertilizer and precipitation regimes in a semi-arid steppe. J Soils Sediment 18:762–774

    Article  CAS  Google Scholar 

  • Tabatabai MA (1994) Soil enzymes. In: Mickelson SH, Bifham JM (eds) Methods of soil analysis, part 2: microbiological and biochemical properties. Soil Science Society of America, Madison, pp 775–833

    Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Tao Z, Shen C, Gao Q, Sun Y, Yi W, Li Y (2006) Soil organic carbon storage and vertical distribution of alpine meadow on the Tibetan plateau. Acta Geograph Sin 61:720–728

    Google Scholar 

  • Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120

    Article  PubMed  Google Scholar 

  • Vamerali T, Ganis A, Bona S, Mosca G (2003) Fibrous root turnover and growth in sugar beet (Beta vulgaris var. saccharifera) as affected by nitrogen shortage. Plant Soil 255:169–177

    Article  CAS  Google Scholar 

  • van den Berg LJ, Dorland E, Vergeer P, Hart MA, Bobbink RJG (2005) Decline of acid-sensitive plant species in heathland can be attributed to ammonium toxicity in combination with low pH. New Phytol 166:551–564

    Article  CAS  PubMed  Google Scholar 

  • van der Heijden MG, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • van der Putten WH, Bradford MA, Pernilla Brinkman E, van de Voorde TFJ, Veen GF, Bailey JK (2016) Where, when and how plant-soil feedback matters in a changing world. Funct Ecol 30:1109–1121

    Article  Google Scholar 

  • Venkatesan S, Senthurpandian VK (2006) Comparison of enzyme activity with depth under tea plantations and forested sites in South India. Geoderma 137:212–216

    Article  CAS  Google Scholar 

  • Wallander H, Nilsson LO, Hagerberg D, Rosengren U (2003) Direct estimates of C : N ratios of ectomycorrhizal mycelia collected from Norway spruce forest soils. Soil Biol Biochem 35:997–999

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wei C, Yu Q, Bai E, Lu X, Li Q, Xia J, Kardol P, Liang W, Wang Z, Han X (2013) Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems. Global Chang Biol 19:3688–3697

    Article  Google Scholar 

  • Xi N, Carrère P, Bloor JMG (2014) Nitrogen form and spatial pattern promote asynchrony in plant Soilresponses to nitrogen inputs in a temperate grassland. Soil Biol Biochem 71:40–47

    Article  CAS  Google Scholar 

  • Xia J, Wan S (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179:428–439

    Article  CAS  PubMed  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

    Article  Google Scholar 

  • Yang YH, Fang JY, Ji CJ, Han WX (2009) Above- and belowground biomass allocation in Tibetan grasslands. J Veg Sci 20:177–184

    Article  Google Scholar 

  • Yang ZL, van Ruijven J, Du GZ (2011) The effects of long-term fertilization on the temporal stability of alpine meadow communities. Plant Soil 345:315–324

    Article  CAS  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

  • Zhang P, Zhou X, Li J, Guo Z, Du G (2015) Space resource utilisation: a novel indicator to quantify species competitive ability for light. Sci Rep 5:16832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao CZ, Zhu LY, Liang J, Yin HJ, Yin CY, Li DD, Zhang NN, Liu Q (2014) Effects of experimental warming and nitrogen fertilization on soil microbial communities and processes of two subalpine coniferous species in eastern Tibetan plateau, China. Plant Soil 382:189–201

    Article  CAS  Google Scholar 

  • Zhou Z, Wang C, Zheng M, Jiang L, Luo Y (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Paolo Nannipieri for valuable comments and assistance in improving this manuscript. This work was supported by National Natural Science Foundation of China (31870435 to S.T.Z) and the National Key Research and Development Program of China (2018YFD0502401 to S.T.Z).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shiting Zhang.

Additional information

Responsible Editor: Elizabeth M Baggs.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 550 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Zhang, S. Nitrogen addition shapes soil enzyme activity patterns by changing pH rather than the composition of the plant and microbial communities in an alpine meadow soil. Plant Soil 440, 11–24 (2019). https://doi.org/10.1007/s11104-019-04054-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04054-5

Keywords

Navigation