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Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea

Authors

  • George F. Wells,

    1. Environmental Engineering and Science Program, Stanford University, Stanford, CA 94305, USA.
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    • These authors contributed equally to this work.

  • Hee-Deung Park,

    1. Environmental Engineering and Science Program, Stanford University, Stanford, CA 94305, USA.
    2. School of Civil, Environmental, and Architectural Engineering, Anam-Dong, Seongbuk-Gu, Seoul 136-713, Korea.
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    • These authors contributed equally to this work.

  • Chok-Hang Yeung,

    1. Environmental Engineering and Science Program, Stanford University, Stanford, CA 94305, USA.
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  • Brad Eggleston,

    1. Palo Alto Regional Water Quality Control Plant, 2501 Embarcadero Way, Palo Alto, CA 94303, USA.
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  • Christopher A. Francis,

    Corresponding author
    1. Department of Environmental Earth System Science, Stanford University, Stanford, CA 94305, USA.
      *E-mail ccriddle@stanford.edu; Tel. (+1) 650 723 9032; Fax (+1) 650 725 3164.
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  • Craig S. Criddle

    Corresponding author
    1. Environmental Engineering and Science Program, Stanford University, Stanford, CA 94305, USA.
      *E-mail ccriddle@stanford.edu; Tel. (+1) 650 723 9032; Fax (+1) 650 725 3164.
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*E-mail ccriddle@stanford.edu; Tel. (+1) 650 723 9032; Fax (+1) 650 725 3164.

Summary

Ammonia-oxidizing bacteria (AOB) have long been considered key to the removal of nitrogen in activated sludge bioreactors. Culture-independent molecular analyses have established that AOB lineages in bioreactors are dynamic, but the underlying operational or environmental factors are unclear. Furthermore, the contribution of ammonia-oxidizing archaea (AOA) to nitrogen removal in bioreactors has not been studied. To this end, we investigated the abundance of AOA and AOB as well as correlations between dynamics in AOB lineages and operational parameters at a municipal wastewater treatment plant sampled weekly over a 1 year period. Quantitative PCR measurements of bacterial and archaeal ammonia monooxygenase subunit A (amoA) genes revealed that the bacterial homologue predominated by at least three orders of magnitude in all samples. Archaeal amoA was only detectable in ∼15% of these samples. Using terminal restriction fragment length polymorphism analysis, we monitored AOB lineages based on amoA genes. The Nitrosomonas europaea lineage and a novel Nitrosomonas-like cluster were the dominant AOB signatures, with a Nitrosospira lineage present at lower relative abundance. These lineages exhibited strong temporal oscillations, with one becoming sequentially dominant over the other. Using non-metric multidimensional scaling and redundancy analyses, we tested correlations between terminal restriction fragment length polymorphism profiles and 20 operational and environmental parameters. The redundancy analyses indicated that the dynamics of AOB lineages correlated most strongly with temperature, dissolved oxygen and influent nitrite and chromium. The Nitrosospira lineage signal had a strong negative correlation to dissolved oxygen and temperature, while the Nitrosomonas-like (negative correlations) and N. europaea lineages (positive correlations) were inversely linked (relative to one another) to influent nitrite and chromium. Overall, this study suggests that AOA may be minor contributors to ammonia oxidation in highly aerated activated sludge, and provides insight into parameters controlling the diversity and dominance of AOB lineages within bioreactors during periods of stable nitrification.

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