Dynamics of nitrification in deep oligotrophic Lake Constance

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2022
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(“Thaumarchaeota”) are important players in nitrification by oxidizing ammonia to nitrite, the first and rate-limiting step of nitrification. They are known to thrive best in oligotrophic environments, where they compete against their bacterial counterparts. Quantitative PCR, meta-genomics, and -transcriptomics were applied to study their abundance and activity throughout an annual cycle in the hypolimnion of deep oligotrophic Lake Constance, Germany. Moreover, nitrification rates were measured with stable isotopes and single-cell ammonia assimilation rates. In the hypo-limnion, a clonal ammonia-oxidizing archaeal population with a mean of 4.3 × 104 amoA copies ml–1 was found which reached a maximum relative abundance of 39% in summer. Phylogenetically, this population is affiliated with a new freshwater-brackish clade, distinct from related marine Nitroso-pumilus relatives. The name “Candidatus Nitrosopumilus limneticus” was proposed for this newly discovered species, which occurs in major inland water bodies around the world. Abundance and expression patterns of Ca. Nitrosopumilus limneticus were one to two orders of magnitude higher than for ammonia-oxidizing bacteria. Genes encoding the individual subunits of the ammonia mono-oxygenase were among the most highly expressed genes, supporting the involvement of the limnic Ca. Nitrosopumilus limneticus in nitrification. Correspondingly, overall nitrification rates of around 6.0 ± 0.9 nmol l–1 d–1 in the hypolimnion can be attributed mainly to this single archaeal species with cell-specific rates of 0.21 ± 0.11 fmol ammonia cell–1 d–1. Furthermore, stable isotope activity measure-ments with 15N-ammonia showed that Nitrososphaeria assimilated significantly more ammonia than other hypolimnic microorganisms. On average, 12% of the total assimilated ammonia by the microbial community in the hypolimnion is taken up by Ca. Nitrosopumilus limneticus. Each year 1.76 × 109 g NH4+ is oxidized by ammonia oxidizers in the hypolimnion of Lake Constance, which corresponds to 11% of N-biomass produced by phytoplankton every year. Autotrophic Nitrososphaeria use hydrogen carbonate for their carbon demand. Based on transcription levels of their carbon fixation genes, Nitrososphaeria are in the same range as nitrite oxidizers, cyanobacteria and an alphaproteobacterial RubisCO cluster in the hypolimnion. The all-encompassing dominant autotroph in the hypolimnion based on transcription levels, was related to a cryptophyte, which is hypothesized to be a symbiont of a ciliate species. Accordingly, Ca. Nitrosopumilus limneticus has less of an impact on the carbon cycle than the nitrogen cycle. In conclusion, this study showed that Ca. Nitrosopumilus limneticus is nearly the sole ammonia oxidizer in oligotrophic Lake Constance, strongly contributing to the removal of ammonia in lake water, and in turn, accomplish an essential ecosystem service for safe drinking water supply.

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ISO 690KLOTZ, Franziska, 2022. Dynamics of nitrification in deep oligotrophic Lake Constance [Dissertation]. Konstanz: Universität Konstanz
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@phdthesis{Klotz2022Dynam-57819,
  year={2022},
  title={Dynamics of nitrification in deep oligotrophic Lake Constance},
  author={Klotz, Franziska},
  address={Konstanz},
  school={Universität Konstanz}
}
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    <dcterms:abstract xml:lang="eng">(“Thaumarchaeota”) are important players in nitrification by oxidizing ammonia to nitrite, the first and rate-limiting step of nitrification. They are known to thrive best in oligotrophic environments, where they compete against their bacterial counterparts. Quantitative PCR, meta-genomics, and -transcriptomics were applied to study their abundance and activity throughout an annual cycle in the hypolimnion of deep oligotrophic Lake Constance, Germany. Moreover, nitrification rates were measured with stable isotopes and single-cell ammonia assimilation rates. In the hypo-limnion, a clonal ammonia-oxidizing archaeal population with a mean of 4.3 × 104 amoA copies ml–1 was found which reached a maximum relative abundance of 39% in summer. Phylogenetically, this population is affiliated with a new freshwater-brackish clade, distinct from related marine Nitroso-pumilus relatives. The name “Candidatus Nitrosopumilus limneticus” was proposed for this newly discovered species, which occurs in major inland water bodies around the world. Abundance and expression patterns of Ca. Nitrosopumilus limneticus were one to two orders of magnitude higher than for ammonia-oxidizing bacteria. Genes encoding the individual subunits of the ammonia mono-oxygenase were among the most highly expressed genes, supporting the involvement of the limnic Ca. Nitrosopumilus limneticus in nitrification. Correspondingly, overall nitrification rates of around 6.0 ± 0.9 nmol l–1 d–1 in the hypolimnion can be attributed mainly to this single archaeal species with cell-specific rates of 0.21 ± 0.11 fmol ammonia cell–1 d–1. Furthermore, stable isotope activity measure-ments with 15N-ammonia showed that Nitrososphaeria assimilated significantly more ammonia than other hypolimnic microorganisms. On average, 12% of the total assimilated ammonia by the microbial community in the hypolimnion is taken up by Ca. Nitrosopumilus limneticus. Each year 1.76 × 109 g NH4+ is oxidized by ammonia oxidizers in the hypolimnion of Lake Constance, which corresponds to 11% of N-biomass produced by phytoplankton every year. Autotrophic Nitrososphaeria use hydrogen carbonate for their carbon demand. Based on transcription levels of their carbon fixation genes, Nitrososphaeria are in the same range as nitrite oxidizers, cyanobacteria and an alphaproteobacterial RubisCO cluster in the hypolimnion. The all-encompassing dominant autotroph in the hypolimnion based on transcription levels, was related to a cryptophyte, which is hypothesized to be a symbiont of a ciliate species. Accordingly, Ca. Nitrosopumilus limneticus has less of an impact on the carbon cycle than the nitrogen cycle. In conclusion, this study showed that Ca. Nitrosopumilus limneticus is nearly the sole ammonia oxidizer in oligotrophic Lake Constance, strongly contributing to the removal of ammonia in lake water, and in turn, accomplish an essential ecosystem service for safe drinking water supply.</dcterms:abstract>
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March 25, 2022
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Konstanz, Univ., Diss., 2022
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