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Distribution of sediment ammonia-oxidizing microorganisms in plateau freshwater lakes

  • Environmental biotechnology
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Abstract

Both ammonia-oxidizing bacteria (AOB) and archaea (AOA) can play important roles in ammonia biotransformation in ecosystems. However, the factors regulating the distribution of these microorganisms in lacustrine ecosystems remain essentially unclear. The present study investigated the effects of geographic location on the distribution of sediment AOA and AOB in 13 freshwater lakes on the Yunnan Plateau (China). The spatial dissimilarity in the abundance and structure of sediment AOA and AOB communities was observed in these plateau lakes. AOA abundance was usually less than AOB abundance, and the AOA/AOB ratio was positively correlated with water depth. Nitrososphaera-like AOA occurred in most of the studied lakes and were dominant in two lakes. Nitrosospira was the dominant AOB species in most of the lakes, while Nitrosomonas showed high abundance only in three lakes. In addition, geographic location was found to affect lake sediment AOB community structure.

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References

  • Abell GCJ, Ross DJ, Keane J, Holmes BH, Robert SS, Keough MJ, Eyre BD, Volkman JK (2014) Niche differentiation of ammonia-oxidising archaea (AOA) and bacteria (AOB) in response to paper and pulp mill effluent. Microb Ecol 67:758–768

    Article  CAS  PubMed  Google Scholar 

  • Auguet JC, Triado-Margarit X, Nomokonova N, Camarero L, Casamayor EO (2012) Vertical segregation and phylogenetic characterization of ammonia-oxidizing archaea in a deep oligotrophic lake. ISME J 6:1786–1797

    Article  PubMed Central  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 

  • Han MQ, Li ZY, Zhang FL (2013) The ammonia oxidizing and denitrifying prokaryotes associated with sponges from different sea areas. Microb Ecol 66:427–436

    Article  CAS  PubMed  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  PubMed Central  CAS  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 

  • 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  PubMed Central  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 

  • Jiang HC, Dong HL, Yu BS, Lv G, Deng SC, Berzins N, Dai MH (2009) Diversity and abundance of ammonia-oxidizing archaea and bacteria in Qinghai Lake, Northwestern China. Geomicrobiol J 26:199–211

    Article  CAS  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 

  • 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 79:4065–4071

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Y, Zhang JX, Zhang XL, Xie SG (2014a) 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 

  • Liu Y, Zhang JX, Zhao L, Li YZ, Yang YY, Xie SG (2014b) Aerobic and nitrite-dependent methane-oxidizing microorganisms in sediments of freshwater lakes on the Yunnan Plateau. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-6141-5

    PubMed Central  Google Scholar 

  • Logares R, Lindstrom ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, Rengefors K, Tranvik L, Bertilsson S (2013) Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J 7:937–948

    Article  PubMed Central  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 Bioinforma 7:371

    Article  Google Scholar 

  • Meyer A, Focks A, Radl V, Welzl G, Schoning I, Schloter M (2014) Influence of land use intensity on the diversity of ammonia oxidizing bacteria and archaea in soils from grassland ecosystems. Microb Ecol 67:161–166

    Article  CAS  PubMed  Google Scholar 

  • Miazga-Rodriguez M, Han S, Yakiwchuk B, Wei K, English C, Bourn S, Bohnert S, Stein LY (2012) Enhancing nitrification at low temperature with zeolite in a mining operations retention pond. Front Microbiol 3:271

    Article  PubMed Central  CAS  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Park HD, Noguera DR (2007) Characterization of two ammonia-oxidizing bacteria isolated from reactors operated with low dissolved oxygen concentrations. J Appl Microbiol 102:1401–1417

    Article  CAS  PubMed  Google Scholar 

  • Pereira E Silva E, Silva MC, Poly F, Guillaumaud N, van Elsas JD, Salles JF (2012) Fluctuations in ammonia oxidizing communities across agricultural soils are driven by soil structure and pH. Front Microbiol 3:77

    Article  PubMed Central  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 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  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  PubMed Central  CAS  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 SY, Wang Y, Feng XJ, Zhai LM, Zhu GB (2011) Quantitative analyses of ammonia-oxidizing Archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Appl Microbiol Biotechnol 90:779–787

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Zhu G, Ye L, Feng X, Op den Camp HJ, Yin C (2012) Spatial distribution of archaeal and bacterial ammonia oxidizers in the littoral buffer zone of a nitrogen-rich lake. J Environ Sci 24:790–799

    Article  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang YF, Gu JD (2014) Effects of allylthiourea, salinity, and pH on ammonia/ammonium-oxidizing prokaryotes in mangrove sediment incubated in laboratory microcosm. Appl Microbiol Biotechnol 98:3257–3274

    Article  CAS  PubMed  Google Scholar 

  • Wang XY, Wang C, Bao LL, Xie SG (2014a) 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 

  • Wang J, Dong H, Wang W, Gu JD (2014b) Reverse-transcriptional gene expression of anammox and ammonia-oxidizing archaea and bacteria in soybean and rice paddy soils of northeast China. Appl Microbiol Biotechnol 98:2675–2686

    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 

  • Xiong JB, Liu YQ, Lin XG, Zhang HY, Zeng J, Hou JZ, Yang YP, Yao TD, Knight R, Chu HY (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:SI 2457–2466

  • Yang J, Jiang HC, Dong HL, Wang HY, Wu G, Hou WG, Liu WG, Zhang CL, Sun YJ, Lai ZP (2013) amoA-encoding archaea and thaumarchaeol in the lakes on the northeastern Qinghai-Tibetan Plateau, China. Front Microbiol 4:329

    PubMed Central  CAS  PubMed  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 

  • 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 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 Y, Hou L, Newell S, Liu M, Zhou J, Zhao H, You L, Cheng X (2014) Community dynamics and activity of ammonia-oxidizing prokaryotes in intertidal sediments of the Yangtze Estuary. Appl Environ Microbiol 80:408–419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

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

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Correspondence to Shuguang Xie.

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Liu, Y., Zhang, J., Zhao, L. et al. Distribution of sediment ammonia-oxidizing microorganisms in plateau freshwater lakes. Appl Microbiol Biotechnol 99, 4435–4444 (2015). https://doi.org/10.1007/s00253-014-6341-z

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  • DOI: https://doi.org/10.1007/s00253-014-6341-z

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