Skip to main content

Advertisement

SpringerLink
Log in

Ammonia- and methane-oxidizing microorganisms in high-altitude wetland sediments and adjacent agricultural soils

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Ammonia oxidation is known to be carried out by ammonia-oxidizing bacteria (AOB) and archaea (AOA), while methanotrophs (methane-oxidizing bacteria (MOB)) play an important role in mitigating methane emissions from the environment. However, the difference of AOA, AOB, and MOB distribution in wetland sediment and adjacent upland soil remains unclear. The present study investigated the abundances and community structures of AOA, AOB, and MOB in sediments of a high-altitude freshwater wetland in Yunnan Province (China) and adjacent agricultural soils. Variations of AOA, AOB, and MOB community sizes and structures were found in water lily-vegetated and Acorus calamus-vegetated sediments and agricultural soils (unflooded rice soil, cabbage soil, and garlic soil and flooded rice soil). AOB community size was higher than AOA in agricultural soils and lily-vegetated sediment, but lower in A. calamus-vegetated sediment. MOB showed a much higher abundance than AOA and AOB. Flooded rice soil had the largest AOA, AOB, and MOB community sizes. Principal coordinate analyses and Jackknife Environment Clusters analyses suggested that unflooded and flooded rice soils had relatively similar AOA, AOB, and MOB structures. Cabbage soil and A. calamus-vegetated sediment had relatively similar AOA and AOB structures, but their MOB structures showed a large difference. Nitrososphaera-like microorganisms were the predominant AOA species in garlic soil but were present with a low abundance in unflooded rice soil and cabbage soil. Nitrosospira-like AOB were dominant in wetland sediments and agricultural soils. Type I MOB Methylocaldum and type II MOB Methylocystis were dominant in wetland sediments and agricultural soils. Moreover, Pearson’s correlation analysis indicated that AOA Shannon diversity was positively correlated with the ratio of organic carbon to nitrogen (p < 0.05). This work could provide some new insights toward ammonia and methane oxidation in soil and wetland sediment ecosystems.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alam MS, Jia ZJ (2012) Inhibition of methane oxidation by nitrogenous fertilizers in a paddy soil. Front Microbiol 3:246

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Auman AJ, Stolyar S, Costello AM, Lidstrom ME (2000) Molecular characterization of methanotrophic isolates from freshwater lake sediment. Appl Environ Microbiol 66:5259–5266

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Avrahami S, Bohannan BJA (2007) Response of Nitrosospira sp. strain AF-Like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. Appl Environ Microbiol 73:1166–1173

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bodelier PLE (2011) Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils. Curr Opin Environ Sustain 3:379–388

    Article  Google Scholar 

  • Bodrossy L, Holmes EM, Holmes AJ, Kovacs KL, Murrell JC (1997) Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov. Arch Microbiol 168:493–503

    Article  CAS  PubMed  Google Scholar 

  • Brown MN, Briones A, Diana J, Raskin L (2013) Ammonia-oxidizing archaea and nitrite-oxidizing nitrospiras in the biofilter of a shrimp recirculating aquaculture system. FEMS Microbiol Ecol 83:17–25

    Article  CAS  PubMed  Google Scholar 

  • Chang CY, Tung HH, Tseng IC, Wu JH, Liu YF, Lin HM (2010) Dynamics of methanotrophic communities in tropical alkaline landfill upland soil. Appl Soil Ecol 46:92–199

    Article  CAS  Google Scholar 

  • Chen X, Zhang LM, Shen JP, Xu ZH, He JZ (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10:1510–1516

    Article  CAS  Google Scholar 

  • Chowdhury TR, Dick RP (2013) Ecology of aerobic methanotrophs in controlling methane fluxes from wetlands. Appl Soil Ecol 65:8–22

    Article  Google Scholar 

  • Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074

    CAS  PubMed Central  PubMed  Google Scholar 

  • Degelmann DM, Borken W, Drake HL, Kolb S (2010) Different atmospheric methane-oxidizing communities in European beech and Norway spruce soils. Appl Environ Microbiol 76:3228–3235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deng YC, Cui XY, Luke C, Dumont MG (2013) Aerobic methanotroph diversity in Riganqiao peatlands on the Qinghai-Tibetan Plateau. Environ Microbiol Rep 5:566–574

    Article  CAS  PubMed  Google Scholar 

  • Dorr N, Glaser B, Kolb S (2010) Methanotrophic communities in Brazilian ferralsols from naturally forested, afforested, and agricultural sites. Appl Environ Microbiol 76:1307–1310

    Article  PubMed Central  PubMed  Google Scholar 

  • Gao JF, Luo X, Wu GX, Li T, Peng YZ (2014) Abundance and diversity based on amoA genes of ammonia-oxidizing archaea and bacteria in ten wastewater treatment systems. Appl Microbiol Biotechnol 98:3339–3354

    Article  CAS  PubMed  Google Scholar 

  • Glaser K, Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S, Sessitsch A (2010) Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol 74:575–591

    Article  CAS  PubMed  Google Scholar 

  • Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574

    Article  CAS  PubMed  Google Scholar 

  • Han B, Chen Y, Abell G, Jiang H, Bodrossy L, Zhao JG, Murrell JC, Xing XH (2009) Diversity and activity of methanotrophs in alkaline soil from a Chinese coal mine. FEMS Microbiol Ecol 70:196–207

    Article  CAS  Google Scholar 

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    CAS  PubMed Central  PubMed  Google Scholar 

  • He R, Wooller MJ, Pohlman JW, Quensen J, Tiedje JM, Leigh MB (2012) Diversity of active aerobic methanotrophs along depth profiles of arctic and subarctic lake water column and sediments. ISME J 6:1937–1948

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Herrmann M, Saunders AM, Schramm A (2009) Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Appl Environ Microbiol 75:3127–3136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hofferle S, Nicol GW, Pal L, Hacin J, Prosser JI, Mandic-Mulec I (2010) Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile. FEMS Microbiol Ecol 74:302–315

    Article  CAS  PubMed  Google Scholar 

  • Hu BL, Liu SA, Shen LD, Zheng P, Xu XY, Lou LP (2012) Effect of different ammonia concentrations on community succession of ammonia-oxidizing microorganisms in a simulated paddy soil column. PLOS One doi:101371/journalpone0044122

  • Iguchi H, Yurimoto H, Sakai Y (2011) Stimulation of methanotrophic growth in cocultures by cobalamin excreted by Rhizobia. Appl Environ Microbiol 77:8509–8515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jacinthe PA, Dick WA, Lal R, Shrestha RK, Bilen S (2014) Effects of no-till duration on the methane oxidation capacity of Alfisols. Biol Fertil Soils 50:477–486

    Article  CAS  Google Scholar 

  • Jia ZJ, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  CAS  PubMed  Google Scholar 

  • Ke XB, Lu YH (2012) Adaptation of ammonia-oxidizing microorganisms to environment shift of paddy field soil. FEMS Microbiol Ecol 80:87–97

    Article  CAS  PubMed  Google Scholar 

  • Knief C, Dunfield PF (2005) Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ Microbiol 7:1307–1317

    Article  CAS  PubMed  Google Scholar 

  • Kolb S, Knief C, Stubner S, Conrad R (2003) Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl Environ Microbiol 69:2423–2429

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li XR, Xiao YP, Ren WW, Liu ZF, Shi JH, Quan ZX (2012) Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River Estuary. J Zhejiang Univ-SCI B 13:769–782

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Y, Zhang JX, Zhang XL, Xie SG (2014) Depth-related changes of sediment ammonia-oxidizing microorganisms in a high-altitude freshwater wetland. Appl Microbiol Biotechnol 98:5697–5707

    Article  CAS  PubMed  Google Scholar 

  • Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform 7:371–384

    Article  Google Scholar 

  • Ma K, Conrad R, Lu YH (2013) Dry/wet cycles change the activity and population dynamics of methanotrophs in rice field soil. Appl Environ Microbiol 79:4932–4939

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mintie AT, Heichen RS, Cromack K, Myrold DD, Bottomley PJ (2003) Ammonia-oxidizing bacteria along meadow-to-forest transects in the Oregon Cascade Mountains. Appl Environ Microbiol 69:3129–3136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611

    Article  CAS  PubMed  Google Scholar 

  • Sims A, Horton J, Gajaraj S, McIntosh S, Miles RJ, Mueller R, Reed R, Hu ZQ (2012) Temporal and spatial distributions of ammonia-oxidizing archaea and bacteria and their ratio as an indicator of oligotrophic conditions in natural wetlands. Water Res 46:4121–4129

    Article  CAS  PubMed  Google Scholar 

  • Singh JS, Kashyap AK (2007) Contrasting pattern of methanotrophs in dry tropical forest soils: effect of soil nitrogen, carbon and moisture. Microbiol Res 162:276–283

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4, molecular evolutionary genetics analysis, MEGA software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420–8425

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vissers EW, Anselmetti FS, Bodelier PLE, Muyzer G, Schleper C, Tourna M, Laanbroek HJ (2013) Temporal and spatial coexistence of archaeal and bacterial amoA genes and gene transcripts in Lake Lucerne. Archaea 2013:289478

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang YF, Gu JD (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl Microbiol Biotechnol 97:7015–7033

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang XY, Wang C, Bao LL, Xie SG (2014) Abundance and community structure of ammonia-oxidizing microorganisms in reservoir sediment and adjacent soils. Appl Microbiol Biotechnol 98:1883–1892

    Article  CAS  PubMed  Google Scholar 

  • Xu YG, Yu WT, Ma Q, Zhou H (2012) Responses of bacterial and archaeal ammonia oxidisers of an acidic luvisols soil to different nitrogen fertilization rates after 9 years. Biol Fertil Soils 48:827–837

    Article  CAS  Google Scholar 

  • Yun JL, Zhuang GQ, Ma AZ, Guo HG, Wang YF, Zhang HX (2012) Community structure, abundance, and activity of methanotrophs in the Zoige Wetland of the Tibetan Plateau. Microb Ecol 63:835–843

    Article  CAS  PubMed  Google Scholar 

  • Yun JL, Yu ZS, Li K, Zhang HX (2013) Diversity, abundance and vertical distribution of methane-oxidizing bacteria (methanotrophs) in the sediments of the Xianghai Wetland, Songnen Plain, northeast China. J Soils Sediments 13:242–252

    Article  CAS  Google Scholar 

  • Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang JX, Zhang XL, Liu Y, Xie SG, Liu YG (2013) Bacterioplankton communities in a high-altitude freshwater wetland. Ann Microbiol. doi:10.1007/s13213-013-0785-8

    Google Scholar 

  • Zhao DY, Luo J, Zeng J, Wang M, Yan WM, Huang R, Wu QLL (2014) Effects of submerged macrophytes on the abundance and community composition of ammonia-oxidizing prokaryotes in a eutrophic lake. Environ Sci Pollut Res 21:389–398

    Article  Google Scholar 

  • Zheng Y, Zhang LM, Zheng YM, Di HJ, He JZ (2008) Abundance and community composition of methanotrophs in a Chinese paddy soil under long-term fertilization practices. J Soils Sediments 8:406–414

    Article  CAS  Google Scholar 

  • Zheng Y, Yang W, Sun X, Wang SP, Rui YC, Luo CY, Guo LD (2012) Methanotrophic community structure and activity under warming and grazing of alpine meadow on the Tibetan Plateau. Appl Microbiol Biotechnol 93:2193–2203

    Article  CAS  PubMed  Google Scholar 

  • Zheng YL, Hou LJ, Liu M, Lu M, Zhao H, Yin GY, Zhou JL (2013) Diversity, abundance, and activity of ammonia-oxidizing bacteria and archaea in Chongming eastern intertidal sediments. Appl Microbiol Biotechnol 97:8351–8363

    Article  CAS  PubMed  Google Scholar 

  • Zheng YL, Hou LJ, Newell S, Liu M, Zhou JL, Zhao H, You LL, Cheng XL (2014) Community dynamics and activity of ammonia-oxidizing prokaryotes in intertidal sediments of the Yangtze Estuary. Appl Environ Microbiol 80:408–419

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by special fund of State Key Joint Laboratory of Environment Simulation and Pollution Control (14Y02ESPCP), the National Natural Science Foundation of China (No. 41222002) and (No. 51279001), and Collaborative Innovation Center for Regional Environmental Quality.

Author information

Authors and Affiliations

  1. State Key Joint Laboratory of Environmental Simulation and Pollution Control, College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, China

    Yuyin Yang, Jingwen Shan, Jingxu Zhang & Shuguang Xie

  2. Key Laboratory of Water and Sediment Sciences (Ministry of Education), College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, China

    Xiaoling Zhang & Yong Liu

Authors
  1. Yuyin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jingwen Shan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jingxu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuguang Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shuguang Xie or Yong Liu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 436 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Shan, J., Zhang, J. et al. Ammonia- and methane-oxidizing microorganisms in high-altitude wetland sediments and adjacent agricultural soils. Appl Microbiol Biotechnol 98, 10197–10209 (2014). https://doi.org/10.1007/s00253-014-5942-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-5942-x

Keywords

Search

Navigation