Skip to main content
SpringerLink
Log in

Responses of soil inhabiting nitrogen-cycling microbial communities to wetland degradation on the Zoige Plateau, China

  • Mountain Environment
  • Published:
Journal of Mountain Science Aims and scope Submit manuscript

Abstract

The wetlands on the Zoige Plateau have experienced serious degradation, with most of the original marsh being converted to marsh meadow or meadow. Based on the 3 wetland degradation stages, we determined the effects of wetland degradation on the structure and relative abundance of nitrogen-cycling (nitrogen-fixing, ammonia-oxidizing, and denitrifying) microbial communities in 3 soil types (intact wetland: marsh soil; early degrading wetland: marsh meadow soil; and degraded wetland: meadow soil) using 454-pyrosequencing. The structure and relative abundance of nitrogen-cycling microbial communities differed in the 3 soil types. Proteobacteria was the predominant phylum in most soil samples but the most abundant soil nitrogen-fixing and denitrifying microbial bacteria differed at the class, order, family, and genus levels among the 3 soil types. At the genus level, the majority of nitrogen-fixing bacterium sequences related to Bradyrhizobium were from marsh and marsh meadow soils; whereas those related to Geobacter originated from meadow soil. The majority of ammonia-oxidizing bacterium sequences related to Nitrosospira were from marsh (except for the 40-60 cm layer), marsh meadow and meadow soils; whereas those related to Candidatus Solibacter originated from 40-60 cm layer of marsh soil. The majority of denitrifying bacterium sequences related to Candidatus Solibacter and Anaeromyxobacter were from marsh and meadow soils; whereas those related to Herbaspirillum originated from meadow soil. The distribution of operational taxonomic units (OTUs) and species were correlated with soil type based upon Venn and Principal Coordinates Analysis (PCoA). Changes in soil type, caused by different water regimes were the most important factors influencing compositional changes in the nitrogen-fixing, ammonia-oxidizing, and denitrifying microbial communities.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bai J, Lu Q, Zhao Q, et al. (2013) Effects of alpine wetland landscapes on regional climate on the Zoige Plateau of China. Advances in Meteorology 2013(5): 1–7. DOI: 10.1155/2013/972430

    Article  Google Scholar 

  • Bodelier PL, Dedysh SN (2013) Microbiology of wetlands. Frontiers in Microbiology 4(4): 79. DOI: 10.3389/fmicb.2013. 00079

    Google Scholar 

  • Botelho GR, Mendonça-Hagler LC (2006) Fluorescent Pseudomonads associated with the rhizosphere of crops: an overview. Brazilian Journal of Microbiology 37(4): 401–416. DOI: 10.1590/S1517-83822006000400001

    Article  Google Scholar 

  • Castañeda LE, Barbosa O (2016) Metagenomic analysis exploring taxonomic and functional diversity of soil microbial communities in Chilean vineyards and surrounding native forests. PeerJ PrePrints 4: e1661v1. DOI: 10.7287/peerj. reprints.1661v1

    Google Scholar 

  • Chen H, Yang G, Peng C, et al. (2014) The carbon stock of alpine peatlands on the Qinghai–Tibetan Plateau during the Holocene and their future fate. Quaternary Science Reviews 95(7): 151–158. DOI: 10.1016/j.quascirev.2014.05.003

    Article  Google Scholar 

  • Chen Z, Wu W, Shao X, et al. (2015) Shifts in abundance and diversity of soil ammonia-oxidizing bcteria and archaea asociated with land restoration in a semi-arid ecosystem. PloS One 10(7): e0132879. DOI: 10.1371/journal.pone.0132879

    Article  Google Scholar 

  • Chu H, Fujii T, Morimoto S, et al. (2007) Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Applied and Environmental Microbiology 73(2): 485–491. DOI: 10.1128/AEM.01536-06

    Article  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, et al. (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiology Ecology 72(3): 386–394. DOI: 10.1111/j.1574-6941.2010.00861.x

    Article  Google Scholar 

  • Diallo MD, Willems A, Vloemans N, et al. (2004) Polymerase chain reaction denaturing gradient gel electrophoresis analysis of the N2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddiana and Balanites aegyptiaca in the dryland part of Senegal. Environmental Microbiology 6(4): 400–415. DOI: 10.1111/j.1462-2920.2004.00577.x

    Article  Google Scholar 

  • Dong L, Meng Y, Wang J, et al. (2014) Evaluation of droplet digital PCR for characterizing plasmid reference material used for quantifying ammonia oxidizers and denitrifiers. Anal Bioanal Chem 406(6): 1701–1712. DOI: 10.1007/s00216-013-7546-1

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19): 2460–2461. DOI: 10.1093/bioinformatics/btq461

    Article  Google Scholar 

  • Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Applied and Environmental Microbiology 71(12): 8335–8343. DOI: 10.1128/AEM.71.12. 8335-8343.2005

    Article  Google Scholar 

  • Fei S, Cui L, He Y, et al. (2006) A background study of the wetland ecosystem research station in the Ruoergai Plateau. Journal of Sichuan Forestry Science and Technology 27(2): 21–29. (In Chinese)

    Google Scholar 

  • Gaby JC, Buckley DH (2014) A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen-fixing bacteria. Database 2014(2): bau001. DOI: 10.1093/database/bau001

    Google Scholar 

  • Gao J, Li X, Cheung A, et al. (2013) Degradation of wetlands on the Qinghai-Tibet Plateau: A comparison of the effectiveness of three indicators. Journal of Mountain Science 10(4): 658–667. DOI: 10.1007/s11629-013-2562-3

    Article  Google Scholar 

  • Gubry-Rangin C, Hai B, Quince C, et al. (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proceedings of the National Academy of Sciences 108(52): 21206–21211. DOI: 10.1073/pnas.1109000108

    Article  Google Scholar 

  • Guo X, Du W, Wang X, et al. (2013) Degradation and structure change of humic acids corresponding to water decline in Zoige peatland, Qinghai-Tibet Plateau. The Science of the Total Environment 445–446C: 231–236. DOI: 10.1016/j.scitotenv.2012.12.048

    Article  Google Scholar 

  • Gutknecht JLM, Goodman RM, Balser TC (2006) Linking soil process and microbial ecology in freshwater wetland ecosystems. Plant and Soil 289(1): 17–34. DOI: 10.1007/ s11104-006-9105-4

    Article  Google Scholar 

  • Gyaneshwar P, Hirsch AM, Moulin L, et al. (2011) Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Molecular Plant-Microbe Interactions 24(11): 1276–1288. DOI: 10.1094 / MPMI-06-11-0172

    Article  Google Scholar 

  • Hallin S, Jones CM, Schloter M, et al. (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. The ISME Journal 3(5): 597–605. DOI: 10.1038/ismej.2008.128

    Article  Google Scholar 

  • Hamersley MR, Howes BL (2002) Control of denitrification in a septage-treating artificial wetland: the dual role of particulate organic carbon. Water Research 36(17): 4415–4427. DOI: 10.1016/s0043-1354(02)00134-3

    Article  Google Scholar 

  • Hathaway SK, Porter MD, Rodríguez LF, et al. (2015) Impact of the contemporary environment on denitrifying bacterial communities. Ecological Engineering 82(4): 469–473. DOI: 10.1016/j.ecoleng.2015.05.005

    Article  Google Scholar 

  • Hawkes CV, Wren IF, Herman DJ, et al. (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecology Letters 8(9): 976–985. DOI: 10.1111/ j.1461-0248.2005.00802.x

    Article  Google Scholar 

  • Hou J, Li L, Zhang S, et al. (2012) Diversity of NosZ gene in three municipal wastewater treatment plants located in different geographic regions. African Journal of Microbiology Research 6(15): 3574–3581. DOI: 10.5897/AJMR11.953

    Google Scholar 

  • Hu GY, Dong ZB, Lu JF, et al. (2012) Driving forces of land use and land cover change (LUCC) in the Zoige Wetland, Qinghai-Tibetan Plateau. Sciences in Cold and Arid Regions 4(5): 422. DOI: 10.3724/sp.j.1226.2012.00422

    Article  Google Scholar 

  • Huo L, Chen Z, Zou Y, et al. (2013) Effect of Zoige alpine wetland degradation on the density and fractions of soil organic carbon. Ecological Engineering 51(1): 287–295. DOI: 10.1016/j.ecoleng.2012.12.020

    Article  Google Scholar 

  • Iribar A, Hallin S, Pérez JMS, et al. (2015) Potential denitrification rates are spatially linked to colonization patterns of nosZ genotypes in an alluvial wetland. Ecological Engineering 80(1): 191–197. DOI: 10.1016/j.ecoleng.2015.02. 002

    Article  Google Scholar 

  • Jesser KJ, Fullerton H, Hager KW, et al. (2015) Quantitative PCR analysis of functional genes in iron-rich microbial mats at an active hydrothermal vent system (Lo'ihi Seamount, Hawai'i). Applied and Environmental Microbiology 81(9): 2976–2984. DOI: 10.1128/AEM.03608-14

    Article  Google Scholar 

  • Jiang Y, Jin C, Sun B (2014) Soil aggregate stratification of nematodes and ammonia oxidizers affects nitrification in an acid soil. Environmental Microbiology 16(10): 3083–3094. DOI: 10.1111/1462-2920.12339

    Article  Google Scholar 

  • Jordan FL, Cantera JJ, Fenn ME, et al. (2005) Autotrophic ammonia-oxidizing bacteria contribute minimally to nitrification in a nitrogen-impacted forested ecosystem. Applied and Environmental Microbiology 71(1): 197–206. DOI: 10.1128/AEM.71.1.197-206.2005

    Article  Google Scholar 

  • Li N, Williams HN (2015) 454 Pyrosequencing reveals diversity of Bdellovibrio and like organisms in fresh and salt water. Antonie van Leeuwenhoek Journal of Microbiology 107(1): 305–311. DOI: 10.1007/s10482-014-0327-9

    Article  Google Scholar 

  • Li ZW, Wang ZY, Brierley G, et al. (2015) Shrinkage of the Ruoergai Swamp and changes to landscape connectivity, Qinghai-Tibet Plateau. Catena 126: 155–163. DOI: 10.1016/j.catena.2014.10.035

    Article  Google Scholar 

  • Liang YX, Yi MG, Chu KY, et al. (2007) The research of the relationship between shrinkage of Zoige's wetlands, deterioration and desertification of Zoige's grasslands and north sandy arid region. Chinese Journal of Nature 29(4): 233–238. (In Chinese)

    Google Scholar 

  • Luan J, Cui L, Xiang C, et al. (2014) Soil carbon stocks and quality across intact and degraded alpine wetlands in Zoige, east Qinghai-Tibet Plateau. Wetlands Ecology and Management 22(4): 427–438. DOI: 10.1007/s11273-014-9344-8

    Article  Google Scholar 

  • Ma K, Liu J, Balkovič J, et al. (2016) Changes in soil organic carbon stocks of wetlands on China's Zoige plateau from 1980 to 2010. Ecological Modelling 327: 18–28. DOI: 10.1016/j.ecolmodel.2016.01.009

    Article  Google Scholar 

  • Mentzer JL, Goodman RM, Balser TC (2006) Microbial response over time to hydrologic and fertilization treatments in a simulated wet prairie. Plant and Soil 284(1–2): 85–100. DOI: 10.1007/s11104-006-0032-1

    Article  Google Scholar 

  • Mirza BS, Potisap C, Nüsslein K, et al. (2014) Response of free-living nitrogen-fixing microorganisms to land use change in the Amazon rainforest. Applied and Environmental Microbiology 8(1): 281–288. DOI: 10.1128/AEM.02362-13

    Article  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, et al. (2001) Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature 411(6840): 948–950. DOI: 10.1038/35082070

    Article  Google Scholar 

  • Orellana LH, Rodriguez-R LM, Higgins S, et al. (2014) Detecting nitrous oxide reductase (nosZ) genes in soil metagenomes: method development and implications for the nitrogen cycle. mBio 5(3): e01193–01114. DOI: 10.1073/pnas.121123810910. 1128/mBio.01193-14

    Article  Google Scholar 

  • Peralta AL, Ludmer S, Kent AD (2013) Hydrologic history influences microbial community composition and nitrogen cycling under experimental drying/wetting treatments. Soil Biology and Biochemistry 66(11): 29–37. DOI: 10.1016/j. soilbio.2013.06.019

    Article  Google Scholar 

  • Petersen DG, Blazewicz SJ, Firestone M, et al. (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environmental microbiology 14(4): 993–1008. DOI: 10.1111/j.1462-2920.2011.02679.x

    Article  Google Scholar 

  • Rivett MO, Buss SR, Morgan P, et al. (2008) Nitrate attenuation in groundwater: a review of biogeochemical controlling processes. Water Research 42(16): 4215–4232. DOI: 10.1016/j. watres.2008.07.020

    Article  Google Scholar 

  • Rosch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied and Environmental Microbiology 68(8): 3818–3829. DOI: 10.1128/aem.68.8.3818-3829.2002

    Article  Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology 63(12): 4704–4712.

    Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6): 1386–1394. DOI: 10.1890/06-0219

    Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75(23): 7537–7541. DOI: 10.1128/AEM.01541-09

    Article  Google Scholar 

  • Shang ZH, Feng QS, Wu GL, et al. (2013) Grasslandification has significant impacts on soil carbon, nitrogen and phosphorus of alpine wetlands on the Tibetan Plateau. Ecological Engineering 58(9): 170–179. DOI: 10.1016/j.ecoleng.2013.06.035

    Article  Google Scholar 

  • Shishido M, Sakamoto K, Yokoyama H, et al. (2008) Changes in microbial communities in an apple orchard and its adjacent bush soil in response to season, land-use, and violet root rot infestation. Soil Biology and Biochemistry 40(6): 1460–1473. DOI: 10.1016/j.soilbio.2007.12.024

    Article  Google Scholar 

  • Throback IN, Enwall K, Jarvis A, et al. (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiology Ecology 49(3): 401–417. DOI: 10.1016/j.femsec. 2004.04.011

    Article  Google Scholar 

  • Tian J, Shu C, Chen H, et al. (2014) Response of archaeal communities to water regimes under simulated warming and drought conditions in Tibetan Plateau wetlands. Journal of Soils and Sediments 15(1): 179–188. DOI: 10.1007/s11368-014-0978-1

    Article  Google Scholar 

  • Walker JK, Egger KN, Henry GH (2008) Long-term experimental warming alters nitrogen-cycling communities but site factors remain the primary drivers of community structure in high arctic tundra soils. The ISME Journal 2(9): 982–995. DOI:10.1038/ismej.2008.52

    Article  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, et al. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73(16): 5261–5267. DOI: 10.1128/AEM.00062-07

    Article  Google Scholar 

  • Wang Q, Quensen JF, Fish JA, et al. (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. mBio 4(5): e00592–00513. DOI: 10.1128/mBio.00592-13.

    Article  Google Scholar 

  • Wardle D, Bardgett R, Klironomos J, et al. (2004) Ecological linkages between aboveground and belowground biota. Science 304(5677): 1629–1633. DOI: 10.1126/science.1094875

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, et al. (2006) Structure analysis of a soil community of predatory bacteria using culture-dependent and culture-independent methods reveals a hitherto undetected diversity of Bdellovibrio-and-like organisms. Environmental Microbiology 8(9): 1667–1673. DOI: 10.1111/j.1462-2920.2006.01052.x

    Article  Google Scholar 

  • Webster G, Embley TM, Prosser JI (2002) Grassland management regimens reduce small-scale heterogeneity and species diversity of β-proteobacterial ammonia oxidizer populations. Applied and Environmental Microbiology 68(1): 20–30. DOI: 10.1128/aem.68.1.20-30.2002

    Article  Google Scholar 

  • Wu LS, Feng S, Nie YY, et al. (2015) Soil cellulase activity and fungal community responses to wetland degradation in the Zoige Plateau, China. Journal of Mountain Science 12(2): 471–482. DOI: 10.1007/s11629-014-3183-1

    Article  Google Scholar 

  • Xiang S, Guo R, Wu N, et al. (2009) Current status and future prospects of Zoige Marsh in Eastern Qinghai-Tibet Plateau. Ecological Engineering 35(4): 553–562. DOI: 10.1016/j. ecoleng. 2008.02.016

    Article  Google Scholar 

  • Yang YX, Wang SY (2001) Human disturbances on mire and peat soils in the Zoige Plateau. Resources Science 23(2): 37–41. (In Chinese)

    Google Scholar 

  • Yu Y, Wang H, Liu J, et al. (2012) Shifts in microbial community function and structure along the successional gradient of coastal wetlands in Yellow River Estuary. European Journal of Soil Biology 49(2): 12–21. DOI: 10.1016/j.ejsobi.2011.08.006

    Article  Google Scholar 

  • Yuan Q, Liu P, Lu Y (2012) Differential responses of nirK-and nirS-carrying bacteria to denitrifying conditions in the anoxic rice field soil. Environmental Microbiology Reports 4(1): 113–122.DOI: 10.1111/j.1758-2229.2011.00311.x

    Article  Google Scholar 

  • Zhang X, Liu H, Xing Z (2011) Challenges and Solutions for Sustainable Land Use in Ruoergai-the Highest Altitude Peatland in Qinhai-Tibetan Plateau, China. Energy Procedia 5(1): 1019–1025. DOI: 10.1016/j.egypro.2011.03.180

    Google Scholar 

  • Zhang Y, Li D, Wang H, et al. (2006) Molecular diversity of nitrogen-fixing bacteria from the Tibetan Plateau, China. FEMS Microbiology Letters 260(2): 134–142. DOI: 10.1111/ j.1574-6968.2006.00317

    Article  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the 11th Five Years Key Programs for Science and Technology Development of China (Grant No. 2007BAC18B03).

Author information

Authors and Affiliations

  1. Key Laboratory of Biological Resource and Ecological Environment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, 610065, China

    Li-sha Wu, Yuan-yang Nie, Zhi-rong Yang & Jie Zhang

  2. College of Medical Technology, Chengdu University of Traditional Chinese Medicine, Chengdu, 611137, China

    Li-sha Wu

Authors
  1. Li-sha Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuan-yang Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhi-rong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jie Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jie Zhang.

Additional information

http://orcid.org/0000-0001-7356-1421

http://orcid.org/0000-0001-7235-0171

http://orcid.org/0000-0002-3355-3168

http://orcid.org/0000-0001-8281-9375

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Ls., Nie, Yy., Yang, Zr. et al. Responses of soil inhabiting nitrogen-cycling microbial communities to wetland degradation on the Zoige Plateau, China. J. Mt. Sci. 13, 2192–2204 (2016). https://doi.org/10.1007/s11629-016-4004-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11629-016-4004-5

Keywords

Search

Navigation