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Depth-related changes of sediment ammonia-oxidizing microorganisms in a high-altitude freshwater wetland

  • Environmental biotechnology
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Abstract

Both ammonia-oxidizing bacteria (AOB) and archaea (AOA) might be the key microorganisms in ammonia conversion in ecosystems. However, the depth-related change of AOA and AOB in sediment ecosystem is still not clear. The relative contribution of AOA and AOB to nitrification in wetland sediment remains also unclear. Moreover, information about ammonia-oxidizing microorganisms in high-altitude freshwater wetland is still lacking. The present study investigated the relative abundances and community structures of AOA and AOB in sediments of a high-altitude freshwater wetland in Yunnan Province (China). Variations of the relative abundances and community structures of AOA and AOB were found in the wetland sediments, dependent on both sampling site and sediment depth. The relative abundances of AOA and AOB (0.04–3.84 and 0.01–0.52 %) and the AOA/AOB ratio (0.12–4.65) showed different depth-related change patterns. AOB community size was usually larger than AOA community size. AOB diversity was usually higher than AOA diversity. AOA diversity decreased with the increase of sediment depth, while AOB diversity showed no obvious link with the sediment depth. Pearson’s correlation analysis showed that AOA diversity had a positive significant correlation with available phosphorus. Nitrosospira-like sequences, with different compositions, predominated in the wetland sediment AOB communities. This work could provide some new insights toward nitrification in freshwater sediment ecosystems.

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References

  • Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662

    Article  PubMed  Google Scholar 

  • Cao HL, Hong YG, Li M, Gu JD (2011a) Diversity and abundance of ammonia-oxidizing prokaryotes in sediments from the coastal Pearl River estuary to the South China Sea. Antonie Van Leeuwenhoek 100:545–556

    Article  PubMed Central  PubMed  Google Scholar 

  • Cao HL, Li M, Hong YG, Gu JD (2011b) Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment. Syst Appl Microbiol 34:513–523

    Article  CAS  PubMed  Google Scholar 

  • Cao HL, Hong YG, Li M, Gu JD (2012) Lower abundance of ammonia oxidizing archaea than ammonia-oxidizing bacteria detected in the subsurface sediments of the Northern South China Sea. Geomicrobiol J 29:332–339

    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 

  • Cheng W, Zhang JX, Wang Z, Wang M, Xie SG (2014) Bacterial communities in sediments of a drinking water reservoir. Ann Microbiol. doi:10.1007/s13213-013-0712-z

    Google Scholar 

  • Dang H, Li J, Zhang X, Li T, Tian F, Jin W (2009) Diversity and spatial distribution of amoA-encoding archaea in the deep-sea sediments of the tropical West Pacific Continental Margin. J Appl Microbiol 106:1482–1493

    Article  CAS  PubMed  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624

    Article  CAS  Google Scholar 

  • Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental actors shaping the ecological niches of ammonia oxidizing archaea. FEMS Microbiol Rev 33:855–869

    Article  CAS  PubMed  Google Scholar 

  • Feng S, Zhang XJ, Wang QF, Wan R, Chen C, Xie SG (2012) Heterogeneity of ammonia-oxidizing community structures in a pilot-scale drinking water biofilter. Int Biodeterior Biodegrad 70:148–152

    Article  CAS  Google Scholar 

  • Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci U S A 105:2134–2139

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374

    Article  CAS  PubMed  Google Scholar 

  • Hou J, Song CL, Cao XY, Zhou YY (2013) Shifts between ammonia-oxidizing bacteria and archaea in relation to nitrification potential across trophic gradients in two large Chinese lakes (Lake Taihu and Lake Chaohu). Water Res 47:2285–2296

    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:10.1371/journalpone0044122

    Google Scholar 

  • Im J, Lee SW, Bodrossy L, Barcelona MJ, Semrau JD (2011) Field application of nitrogen and phenylacetylene to mitigate greenhouse gas emissions from landfill cover soils: effects on microbial community structure. Appl Microbiol Biotechnol 89:189–200

    Article  CAS  PubMed  Google Scholar 

  • Jung J, Yeom J, Kim J, Han J, Lim HS, Park H, Hyun S, Park W (2011) Change in gene abundance in the nitrogen biogeochemical cycle with temperature and nitrogen addition in Antarctic soils. Res Microbiol 162:1018–1026

    Article  CAS  PubMed  Google Scholar 

  • Kim JG, Jung MY, Park SJ, Rijpstra WIC, Damste JSS, Madsen EL, Min D, Kim JS, Kim GJ, Rhee SK (2012) Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I1b from an agricultural soil. Environ Microbiol 14:1528–1543

    Article  CAS  PubMed  Google Scholar 

  • Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  Google Scholar 

  • Li M, Cao HL, Hong YG, Gu JD (2011) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia oxidizing bacteria (AOB) in mangrove sediments. Appl Microbiol Biotechnol 89:1243–1254

    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 L, Peng Y, Zheng XH, Xiao L, Yang LY (2010) Vertical structure of bacterial and archaeal communities within the sediment of a eutrophic lake as revealed by culture-independent methods. J Freshw Ecol 25:565–573

    Article  Google Scholar 

  • Liu S, Shen L, Lou L, Tian G, Zheng P, Hu B (2013) Spatial distribution and factors shaping the niche segregation of ammonia-oxidizing microorganisms in the Qiantang River, China. Appl Environ Microbiol 9:4065–4071

    Article  Google Scholar 

  • Long X, Chen CR, Xu ZH, Oren R, He JZ (2012) Abundance and community structure of ammonia-oxidizing bacteria and archaea in a temperate forest ecosystem under ten-years elevated CO2. Soil Biol Biochem 46:163–171

    Article  CAS  Google Scholar 

  • Moin NS, Nelson KA, Bush A, Bernhard AE (2009) Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl Environ Microbiol 75:7461–7468

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park SJ, Park BJ, Rhee SK (2008) Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 12:605–615

    Article  CAS  PubMed  Google Scholar 

  • Purkhold U, Wagner M, Timmermann G, Pommerening-Roser A, Koops HP (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol 53:1485–1494

    Article  CAS  PubMed  Google Scholar 

  • Sakami T (2012) Distribution of ammonia-oxidizing archaea and bacteria in the surface sediments of Matsushima Bay in relation to environmental variables. Microbes Environ 27:61–66

    Article  PubMed  Google Scholar 

  • Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10:1068–1079

    Article  CAS  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 

  • Shivaji S, Kumari K, Kishore KH, Pindi PK, Rao PS, Srinivas TNR, Asthana R, Ravindra R (2011) Vertical distribution of bacteria in a lake sediment from Antarctica by culture-independent and culture-dependent approaches. Res Microbiol 162:191–203

    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 

  • Suwa Y, Sumino T, Noto K (1997) Phylogenetic relationships of activated sludge isolates of ammonia oxidizers with different sensitivities to ammonium sulfate. J Gen Appl Microbiol 43:373–379

    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 

  • van der Wielen PWJJ, Voost S, van der Kooij D (2009) Ammonia-oxidizing bacteria and archaea in groundwater treatment and drinking water distribution systems. Appl Environ Microbiol 75:4687–4695

    Article  PubMed Central  PubMed  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  CAS  PubMed  Google Scholar 

  • Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071

    Article  CAS  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 YF, Feng YY, Ma XJ, Gu JD (2013) Seasonal dynamics of ammonia/ammonium-oxidizing prokaryotes in oxic and anoxic wetland sediments of subtropical coastal mangrove. Appl Microbiol Biotechnol 97:7919–7934

    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 

  • Wu YC, Xiang Y, Wang JJ, Zhong JC, He JZ, Wu QLL (2010) Heterogeneity of archaeal and bacterial ammonia oxidizing communities in Lake Taihu, China. Environ Microbiol Rep 2:569–576

    Article  CAS  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 XQ, Yang LY, Yu ZY, Peng NY, Xiao L, Yin DQ, Qin BQ (2008) Characterization of depth-related microbial communities in lake sediment by denaturing gradient gel electrophoresis of amplified 16S rRNA fragments. J Environ Sci 20:224–230

    Article  Google Scholar 

  • Zhao DY, Zeng J, Wan WH, Liang HD, Huang R, Wu QLL (2013) Vertical distribution of ammonia-oxidizing archaea and bacteria in sediments of a eutrophic lake. Curr Microbiol 67:327–332

    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 

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Nos. 51279001 and 41222002).

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Correspondence to Shuguang Xie.

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Liu, Y., Zhang, J., Zhang, X. et al. Depth-related changes of sediment ammonia-oxidizing microorganisms in a high-altitude freshwater wetland. Appl Microbiol Biotechnol 98, 5697–5707 (2014). https://doi.org/10.1007/s00253-014-5651-5

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