Skip to main content
SpringerLink
Log in

Population and diversity of ammonia-oxidizing archaea and bacteria in a pollutants’ receiving area in Hangzhou Bay

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

Abstract

The community structure of ammonia-oxidizing microorganisms is sensitive to various environmental factors, including pollutions. In this study, real-time PCR and 454 pyrosequencing were adopted to investigate the population and diversity of ammonia-oxidizing archaea (AOA) and bacteria (AOB) temporally and spatially in the sediments of an industrial effluent receiving area in the Qiantang River’s estuary, Hangzhou Bay. The abundances of AOA and AOB amoA genes fluctuated in 105–107 gene copies per gram of sediment; the ratio of AOA amoA/AOB amoA ranged in 0.39–5.52. The AOA amoA/archaeal 16S rRNA, AOB amoA/bacterial 16S rRNA, and AOA amoA/AOB amoA were found to positively correlate with NH4 +-N concentration of the seawater. Nitrosopumilus cluster and Nitrosomonas-like cluster were the dominant AOA and AOB, respectively. The community structures of both AOA and AOB in the sediments exhibited significant seasonal differences rather than spatial changes in the effluent receiving area. The phylogenetic distribution of AOB in this area was consistent with the wastewater treatment plants (WWTPs) discharging the effluent but differed from the Qiantang River and other estuaries, which might be an outcome of long-term effluent discharge.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del tobari, Mexico. Appl Environ Microbiol 72(12):7767–7777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernhard AE, Landry ZC, Blevins A, de la Torre JR, Giblin AE, Stahl DA (2010) Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol 76(4):1285–1289

    Article  CAS  PubMed  Google Scholar 

  • Bouskill NJ, Eveillard D, Chien D, Jayakumar A, Ward BB (2012) Environmental factors determining ammonia-oxidizing organism distribution and diversity in marine environments. Environ Microbiol 14(3):714–729

    Article  CAS  PubMed  Google Scholar 

  • Boyle-Yarwood SA, Bottomley PJ, Myrold DD (2008) Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microbiol 10(11):2956–2965

    Article  CAS  PubMed  Google Scholar 

  • 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(7):660–662

    Article  PubMed  Google Scholar 

  • Cao H, Hong Y, Li M, Gu J-D (2011) Diversity and abundance of ammonia-oxidizing prokaryotes in sediments from the coastal Pearl River estuary to the South China Sea. Anton Leeuw Int J G 100(4):545–556

    Article  Google Scholar 

  • Cao H, Hong Y, Li M, Gu J-D (2012) Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea. Appl Microbiol and Biot 94(1):247–259

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christman GD, Cottrell MT, Popp BN, Gier E, Kirchman DL (2011) Abundance, diversity, and activity of ammonia-oxidizing prokaryotes in the coastal Arctic Ocean in summer and winter. Appl Environ Microbiol 77(6):2026–2034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Flood M, Frabutt D, Floyd D, Powers A, Ezegwe U, Devol A, Tiquia-Arashiro SM (2015) Ammonia-oxidizing bacteria and archaea in sediments of The Gulf of Mexico. Environ Technol 36(1):124–135

    Article  CAS  PubMed  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. P Natl Acad Sci USA 102(41):14683–14688

    Article  CAS  Google Scholar 

  • Gao J-F, Luo X, Wu G-X, Li T, Peng Y-Z (2013) Quantitative analyses of the composition and abundance of ammonia-oxidizing archaea and ammonia-oxidizing bacteria in eight full-scale biological wastewater treatment plants. Bioresource Technol 138:285–296

    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. P Natl Acad Sci USA 105(6):2134–2139

    Article  CAS  Google Scholar 

  • Hayden CJ, Beman JM (2014) High abundances of potentially active ammonia-oxidizing bacteria and archaea in oligotrophic, high-altitude lakes of the Sierra Nevada, California, USA. PLoS one 9(11):e111560

    Article  PubMed  PubMed Central  Google Scholar 

  • He J-Z, Shen J-P, Zhang L-M, Zhu Y-G, Zheng Y-M, Xu M-G, Di H (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(9):2364–2374

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Dong H, Yu B, Lv G, Deng S, Berzins N, Dai M (2009) Diversity and abundance of ammonia-oxidizing archaea and bacteria in Qinghai Lake, Northwestern China. Geomicrobiol J 26(3):199–211

    Article  CAS  Google Scholar 

  • Jin T, Zhang T, Ye L, Lee OO, Wong YH, Qian PY (2011) Diversity and quantity of ammonia-oxidizing archaea and bacteria in sediment of the Pearl River Estuary, China. Appl Microbiol and Biot 90(3):1137–1145

    Article  CAS  Google Scholar 

  • Junier P, Kim OS, Molina V, Limburg P, Junier T, Imhoff JF, Witzel K-P (2008) Comparative in silico analysis of PCR primers suited for diagnostics and cloning of ammonia monooxygenase genes from ammonia-oxidizing bacteria. FEMS Microbiol Ecol 64(1):141–152

    Article  CAS  PubMed  Google Scholar 

  • Klotz MG, Alzerreca J, Norton JM (1997) A gene encoding a membrane protein exists upstream of the amoA/amoB genes in ammonia oxidizing bacteria: A third member of the amo operon? FEMS Microbiol Lett 150(1):65–73

    Article  CAS  PubMed  Google Scholar 

  • Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437(7058):543–546

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. P Natl Acad Sci USA 108(38):15892–15897

    Article  CAS  Google Scholar 

  • Limpiyakorn T, Sonthiphand P, Rongsayamanont C, Polprasert C (2011) Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants. Bioresource Technol 102(4):3694–3701

    Article  CAS  Google Scholar 

  • Liu L, Huang X, Cao W, Yang Y (2012) Pollution load characteristics of the Hangzhou Bay and its surrounding areas. Ocean Dev Manage 5:108–112(In Chinese)

    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(13):4065–4071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magalhaes CM, Machado A, Bordalo AA (2009) Temporal variability in the abundance of ammonia-oxidizing bacteria vs. archaea in sandy sediments of the Douro River estuary, Portugal. Aquatic Microb Ecol 56(1):13–23

    Article  Google Scholar 

  • Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461(7266):976–981

    Article  CAS  PubMed  Google Scholar 

  • Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10(11):3002–3016

    Article  CAS  PubMed  Google Scholar 

  • Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart G-J, Damste JSS (2011) Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J 5(12):1896–1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66(12):5368–5382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puthiya Veettil V, Abdulaziz A, Chekidhenkuzhiyil J, Kalanthingal Ramkollath L, Karayadi Hamza F, Kizhakkepat Kalam B, Kallungal Ravunnikutty M, Nair S (2015) Bacterial domination over archaea in ammonia oxidation in a monsoon-driven tropical estuary. Microb Ecol 69(3):544–553

    Article  CAS  PubMed  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. Appl Environ Microbiol 63(12):4704–4712

    CAS  PubMed  PubMed Central  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(4):1068–1079

    Article  CAS  PubMed  Google Scholar 

  • Sayavedra-Soto LA, Hommes NG, Alzerreca JJ, Arp DJ, Norton JM, Klotz MG (1998) Transcription of the amoC, amoA and amoB genes in Nitrosomonas europaea and Nitrosospira sp, NpAV. FEMS Microbiol Lett 167(1):81–88

    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(23):7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sims A, Horton J, Gajaraj S, McIntosh S, Miles RJ, Mueller R, Reed R, Hu Z (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(13):4121–4129

    Article  CAS  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(5667):66–74

    Article  CAS  PubMed  Google Scholar 

  • Wertz S, Leigh AKK, Grayston SJ (2012) Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol Ecol 79(1):142–154

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Xiang Y, Wang J, Zhong J, He J, Wu QL (2010) Heterogeneity of archaeal and bacterial ammonia-oxidizing communities in Lake Taihu, China. Environ Microbiol Rep 2(4):569–576

    Article  CAS  PubMed  Google Scholar 

  • Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S, Damste JSS (2006) Archaeal nitrification in the ocean. P Natl Acad Sci USA 103(33):12317–12322

    Article  CAS  Google Scholar 

  • Zhang T, Ye L, Tong AHY, Shao M-F, Lok S (2011) Ammonia-oxidizing archaea and ammonia-oxidizing bacteria in six full-scale wastewater treatment bioreactors. Appl Microbiol and Biot 91(4):1215–1225

    Article  CAS  Google Scholar 

  • Zhang Y, Chen L, Dai T, Sun R, Wen D (2015a) Ammonia manipulates the ammonia oxidizing archaea and bacteria in the coastal sediment-water microcosms. Appl Microbiol and Biot 99(15):6481–6491

    Article  CAS  Google Scholar 

  • Zhang Y, Chen L, Sun R, Dai T, Tian J, Wen D (2015b) Ammonia-oxidizing bacteria and archaea in wastewater treatment plant sludge and nearby coastal sediment in an industrial area in China. Appl Microbiol and Biot 99(10):4495–4507

    Article  CAS  Google Scholar 

  • Zhang Y, Chen L, Sun R, Dai T, Tian J, Zheng W, Wen D (2016) Temporal and spatial changes of microbial community in an industrial effluent receiving area in Hangzhou Bay. J Environ Sci

  • Zhao D, Luo J, Wang J, Huang R, Guo K, Li Y, Wu QL (2015) The influence of land use on the abundance and diversity of ammonia oxidizers. Curr Microbiol 70(2):282–289

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Hou L, Liu M, Lu M, Zhao H, Yin G, Zhou J (2013) Diversity, abundance, and activity of ammonia-oxidizing bacteria and archaea in chongming eastern intertidal sediments. Appl Microbiol and Biot 97(18):8351–8363

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Zhongyuan Zheng, Jing Zhang, Zhichao Li, and Chengfeng Zhang from Peking University, Cong Liu from Tsinghua University, and Yin Zhang from Shanghai Normal University for helping in the samples collection.

Author information

Author notes

  1. Renhua Sun

    Present address: Rural Energy & Environment Agency, Ministry of Agriculture, Beijing, 100125, China

Authors and Affiliations

  1. School of Environment, Tsinghua University, Beijing, 100084, China

    Yan Zhang, Lujun Chen & Jinping Tian

  2. Zhejiang Provincial Key Laboratory of Water Science and Technology, Department of Environmental Technology and Ecology, Yangtze Delta Region Institute of Tsinghua University, Jiaxing, Zhejiang, 314050, China

    Lujun Chen & Wei Zheng

  3. College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, China

    Renhua Sun, Tianjiao Dai & Donghui Wen

Authors
  1. Yan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lujun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Renhua Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tianjiao Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinping Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wei Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Donghui Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Donghui Wen.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Funding

This study was supported by a General Project (No. 51,178,002) granted by the National Natural Science Foundation of China.

Conflict of interest

All contributing authors declare no conflicts of interest.

Electronic supplementary material

ESM 1

(PDF 595 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Chen, L., Sun, R. et al. Population and diversity of ammonia-oxidizing archaea and bacteria in a pollutants’ receiving area in Hangzhou Bay. Appl Microbiol Biotechnol 100, 6035–6045 (2016). https://doi.org/10.1007/s00253-016-7421-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7421-z

Keywords

Search

Navigation