Skip to main content
Log in

Increase in ammonia-oxidizing microbe abundance during degradation of alpine meadows may lead to greater soil nitrogen loss

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Alpine meadows on the Tibetan Plateau have experienced severe degradation in recent decades. Although the effects of alpine meadow degradation on soil properties have been well documented, there is still a paucity of knowledge regarding the responses of nitrogen-cycling microbes (NCMs) to degradation and their links to the changes in soil properties. Here, we systematically determined the effects of degraded patch formation on soil properties (i.e., total carbon, total nitrogen, ammonium nitrogen, nitrate nitrogen, available phosphorus, dissolved organic carbon, moisture, δ15N, δ13C, and pH) and NCMs (based on nifH, amoA, narG, nirK, and nirS genes and their transcripts) across three Tibetan alpine meadows at different degradation stages. Results showed that compared to the original grassed patches, the contents of most soil nutrients (e.g., carbon, nitrogen, and phosphorus) were significantly decreased in the degraded patches across the study sites. Degraded patches also tended to have higher soil δ15N values and nitrate contents. Among the aforementioned NCMs, soil diazotrophs and denitrifiers only showed weak responses to the patch formation, while ammonia-oxidizing microbes showed the highest consistency and sensitivity in response to the patch formation across the study sites. The abundance of amoA gene and archaeal amoA mRNA significantly increased in the degraded patches, and they were positively correlated with soil δ15N values and nitrate nitrogen contents, but negatively correlated with soil total nitrogen and inorganic nitrogen contents. These results suggest that the increased ammonia-oxidizing microbial abundance may be an important driver of soil nitrogen loss during degraded patch formation in alpine meadows.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Almaraz M, Porder S (2016) Reviews and syntheses: measuring ecosystem nitrogen status—a comparison of proxies. Biogeosciences 13(18):5395–5403

    Article  Google Scholar 

  • Bai ZG, Dent DL, Olsson L, Schaepman ME (2008) Proxy global assessment of land degradation. Soil Use Manag 24(3):223–234

    Article  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5(5):908–917

    Article  Google Scholar 

  • Chalk PM, He JZ, Peoples MB, Chen D (2017) 15N2 as a tracer of biological N2 fixation: a 75-year retrospective. Soil Biol Biochem 106:36–50

    Article  Google Scholar 

  • Che RX, Deng YC, Wu YB, Zhang J, Wang F, Tang L, Li LF, Ma S, Liu HK, Zhao X, Wang YF, Hao YB, Cui XY (2017) Relationships between biological nitrogen fixation and available nitrogen at scales from molecular to community level. Chin J Ecol 36(1):224–232

    Google Scholar 

  • Chen JJ, Yi SH, Qin Y (2017) The contribution of plateau pika disturbance and erosion on patchy alpine grassland soil on the Qinghai-Tibetan Plateau: implications for grassland restoration. Geoderma 297:1–9

    Article  Google Scholar 

  • Cui XF, Graf HF (2009) Recent land cover changes on the Tibetan Plateau: a review. Clim Change 94(1):47–61

    Article  Google Scholar 

  • Di HJ, Cameron KC (2002a) Nitrate leaching in temperate agroecosystems: sources, factors and mitigating strategies. Nutr Cycl Agroecosyst 64(3):237–256

    Article  Google Scholar 

  • Di HJ, Cameron KC (2002b) The use of a nitrification inhibitor, dicyandiamide (DCD), to decrease nitrate leaching and nitrous oxide emissions in a simulated grazed and irrigated grassland. Soil Use Manag 18(4):395–403

    Article  Google Scholar 

  • Dong SK, Wen L, Li YY, Wang XX, Zhu L, Li XY (2012) Soil-quality effects of grassland degradation and restoration on the Qinghai-Tibetan Plateau. Soil Sci Soc Am J 76(6):2256–2264

    Article  Google Scholar 

  • Dong SK, Wang XX, Liu SL, Li YY, Su XK, Wen L, Zhu L (2015) Reproductive responses of alpine plants to grassland degradation and artificial restoration in the Qinghai-Tibetan Plateau. Grass Forage Sci 70(2):229–238

    Article  Google Scholar 

  • Dong JF, Cui XY, Wang SP, Wang F, Pang Z, Xu N, Zhao GQ, Wang SP (2016) Changes in biomass and quality of alpine steppe in response to N & P fertilization in the Tibetan Plateau. PLoS ONE 11(5):e0156146

    Article  Google Scholar 

  • Gaby JC, Buckley DH (2011) A global census of nitrogenase diversity. Environ Microbiol 13(7):1790–1799

    Article  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, Vorosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70(2):153–226

    Article  Google Scholar 

  • Hall SJ, Weintraub SR, Bowling DR (2016) Scale-dependent linkages between nitrate isotopes and denitrification in surface soils: implications for isotope measurements and models. Oecologia 181(4):1221–1231

    Article  Google Scholar 

  • Han L, Shang Z, Ren G, Wang Y, Ma Y, Li X, Long R (2011) The responses of plant and soil in the “black soil beach” on the Tibetan Plateau to the changes of degradation patch areas. Acta Prataculturae Sin 20(1):1–6

    Google Scholar 

  • He SY, Richards K (2015) Impact of meadow degradation on soil water status and pasture management—a case study in Tibet. Land Degrad Dev 26(5):468–479

    Article  Google Scholar 

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55(1):485–529

    Article  Google Scholar 

  • Kuzyakov Y, Xu XL (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198(3):656–669

    Article  Google Scholar 

  • Lal R (2003) Soil erosion and the global carbon budget. Environ Int 29(4):437–450

    Article  Google Scholar 

  • Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25

    Article  Google Scholar 

  • Li YY, Dong SK, Wen L, Wang XX, Wu Y (2013) The effects of fencing on carbon stocks in the degraded alpine grasslands of the Qinghai-Tibetan Plateau. J Environ Manag 128:393–399

    Article  Google Scholar 

  • Li YY, Dong SK, Wen L, Wang XX, Wu Y (2014) Soil carbon and nitrogen pools and their relationship to plant and soil dynamics of degraded and artificially restored grasslands of the Qinghai-Tibetan Plateau. Geoderma 213:178–184

    Article  Google Scholar 

  • Li YY, Dong SK, Liu SL, Zhou HK, Gao QZ, Cao GM, Wang XX, Su XK, Zhang Y, Tang L, Zhao HD, Wu XY (2015) Seasonal changes of CO2, CH4 and N2O fluxes in different types of alpine grassland in the Qinghai-Tibetan Plateau of China. Soil Biol Biochem 80:306–314

    Article  Google Scholar 

  • Li Y, Wang S, Jiang L, Zhang L, Cui S, Meng F, Wang Q, Li X, Zhou Y (2016) Changes of soil microbial community under different degraded gradients of alpine meadow. Agric Ecosyst Environ 222:213–222

    Article  Google Scholar 

  • Lin L, Li YK, Xu XL, Zhang FW, Du YG, Liu SL, Guo XW, Cao GM (2015) Predicting parameters of degradation succession processes of Tibetan Kobresia grasslands. Solid Earth 6(4):1237–1246

    Article  Google Scholar 

  • Lu XY, Yan Y, Sun J, Zhang XK, Chen YC, Wang XD, Cheng GW (2015) Carbon, nitrogen, and phosphorus storage in alpine grassland ecosystems of Tibet: effects of grazing exclusion. Ecol Evol 5(19):4492–4504

    Article  Google Scholar 

  • Mnich ME, Houlton BZ (2016) Evidence for a uniformly small isotope effect of nitrogen leaching loss: results from disturbed ecosystems in seasonally dry climates. Oecologia 181(2):323–333

    Article  Google Scholar 

  • Ollivier J, Towe S, Bannert A, Hai B, Kastl EM, Meyer A, Su MX, Kleineidam K, Schloter M (2011) Nitrogen turnover in soil and global change. FEMS Microbiol Ecol 78(1):3–16

    Article  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department Of Agriculture Cirular 939, Washington

    Google Scholar 

  • Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20(11):523–531

    Article  Google Scholar 

  • Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Bio Evol 21(3):541–554

    Article  Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512

    Article  Google Scholar 

  • Ren GH, Shang ZH, Long RJ, Hou Y, Deng B (2013) The relationship of vegetation and soil differentiation during the formation of black-soil-type degraded meadows in the headwater of the Qinghai-Tibetan Plateau, China. Environ Earth Sci 69(1):235–245

    Article  Google Scholar 

  • Stahl DA, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101

    Article  Google Scholar 

  • Subbarao GV, Yoshihashi T, Worthington M, Nakahara K, Ando Y, Sahrawat KL, Rao IM, Lata JC, Kishii M, Braun HJ (2015) Suppression of soil nitrification by plants. Plant Sci 233:155–164

    Article  Google Scholar 

  • Tang L, Dong SK, Sherman R, Liu SL, Liu QR, Wang XX, Su XK, Zhang Y, Li YY, Wu Y, Zhao HD, Zhao C, Wu XY (2015) Changes in vegetation composition and plant diversity with rangeland degradation in the alpine region of Qinghai-Tibet Plateau. Rangel J 37(1):107–115

    Article  Google Scholar 

  • Thamdrup B (2012) New pathways and processes in the global nitrogen cycle. Annu Rev Ecol Evol Syst 43:407–428

    Article  Google Scholar 

  • Wang WY, Wang QJ, Wang CY, Shi HL, Li Y, Wang G (2005) The effect of land management on carbon and nitrogen status in plants and soils of alpine meadows on the Tibetan plateau. Land Degrad Dev 16(5):405–415

    Article  Google Scholar 

  • Wang C, Wang X, Liu D, Wu H, Lu X, Fang Y, Cheng W, Luo W, Jiang P, Shi J, Yin H, Zhou J, Han X, Bai E (2014) Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat Commun 5:4799

    Article  Google Scholar 

  • Wang XX, Dong SK, Sherman R, Liu QR, Liu SL, Li YY, Wu Y (2015a) A comparison of biodiversity-ecosystem function relationships in alpine grasslands across a degradation gradient on the Qinghai-Tibetan Plateau. Rangel J 37(1):45–55

    Article  Google Scholar 

  • Wang Y, Xu Z, Zheng J, Abdullah KM, Zhou Q (2015b) Delta 15N of soil nitrogen pools and their dynamics under decomposing leaf litters in a suburban native forest subject to repeated prescribed burning in southeast Queensland, Australia. J Soils Sediment 15(5):1063–1074

    Article  Google Scholar 

  • Wang ZQ, Zhang YZ, Yang Y, Zhou W, Gang CC, Zhang Y, Li JL, An R, Wang K, Odeh I, Qi JG (2016) Quantitative assess the driving forces on the grassland degradation in the Qinghai-Tibet Plateau, in China. Ecol Inform 33:32–44

    Article  Google Scholar 

  • Wen L, Dong SK, Li YY, Li XY, Shi JJ, Wang YL, Liu DM, Ma YS (2013a) Effect of degradation intensity on grassland ecosystem services in the alpine region of Qinghai-Tibetan Plateau, China. PLoS ONE 8(3):e58432

    Article  Google Scholar 

  • Wen L, Dong SK, Li YY, Wang XX, Li XY, Shi JJ, Dong QM (2013b) The impact of land degradation on the C pools in alpine grasslands of the Qinghai-Tibet Plateau. Plant Soil 368(1–2):329–340

    Article  Google Scholar 

  • Wessen E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45(3):193–200

    Article  Google Scholar 

  • Wu RG, Tiessen H (2002) Effect of land use on soil degradation in alpine grassland soil, China. Soil Sci Soc Am J 66(5):1648–1655

    Article  Google Scholar 

  • Wu GL, Ren GH, Dong QM, Shi JJ, Wang YL (2014) Above- and belowground response along degradation gradient in an alpine grassland of the Qinghai-Tibetan Plateau. Clean Soil Air Water 42(3):319–323

    Article  Google Scholar 

  • Xiong DP, Shi PL, Sun YL, Wu JS, Zhang XZ (2014) Effects of grazing exclusion on plant productivity and soil carbon, nitrogen storage in alpine meadows in northern Tibet, China. Chin Geogr Sci 24(4):488–498

    Article  Google Scholar 

  • Zaman M, Nguyen ML, Blennerhassett JD, Quin BF (2008) Reducing NH3, N2O and NO3–N losses from a pasture soil with urease or nitrification inhibitors and elemental S-amended nitrogenous fertilizers. Biol Fertil Soils 44(5):693–705

    Article  Google Scholar 

  • Zhalnina K, de Quadros PD, Camargo FAO, Triplett EW (2012) Drivers of archaeal ammonia-oxidizing communities in soil. Front Microbiol 3:210

    Article  Google Scholar 

  • Zhang L, Unteregelsbacher S, Hafner S, Xu X, Schleuss PM, Miehe G, Kuzyakov Y (2017) Fate of organic and inorganic nitrogen in crusted and non-crusted Kobresia grasslands. Land Degrad Dev 28(1):166–174

    Article  Google Scholar 

  • Zhao HD, Liu SL, Dong SK, Su XK, Wang XX, Wu XY, Wu L, Zhang X (2015) Analysis of vegetation change associated with human disturbance using MODIS data on the rangelands of the Qinghai-Tibet Plateau. Rangel J 37(1):77–87

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB15010201), National Natural Science Foundation of China (41230750), National Basic Research Program (2013CB956000), and National Key Research and Development Program of China (2016YFC0501800). We sincerely appreciate the constructive suggestions from Prof. Zhongjun Jia and Dr. Yang Li regarding preparation of the manuscript. Rongxiao Che was also supported by a Griffith University Postgraduate Research Scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaoyong Cui.

Additional information

Responsible Editor: Christine Hawkes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 45 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Che, R., Wang, F., Wang, W. et al. Increase in ammonia-oxidizing microbe abundance during degradation of alpine meadows may lead to greater soil nitrogen loss. Biogeochemistry 136, 341–352 (2017). https://doi.org/10.1007/s10533-017-0399-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-017-0399-5

Keywords

Navigation