Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment

Katharina Kitzinger, Cory C. Padilla, Hannah K. Marchant*, Philipp F. Hach, Craig W. Herbold, Abiel T. Kidane, Martin Könneke, Sten Littmann, Maria Mooshammer, Jutta Niggemann, Sandra Petrov, Andreas Richter, Frank J. Stewart, Michael Wagner, Marcel M.M. Kuypers, Laura A. Bristow

*Corresponding author for this work

Research output: Contribution to journalLetterResearchpeer-review

Abstract

Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant marine microorganisms1. These organisms thrive in the oceans despite ammonium being present at low nanomolar concentrations2,3. Some Thaumarchaeota isolates have been shown to utilize urea and cyanate as energy and N sources through intracellular conversion to ammonium4–6. Yet, it is unclear whether patterns observed in culture extend to marine Thaumarchaeota, and whether Thaumarchaeota in the ocean directly utilize urea and cyanate or rely on co-occurring microorganisms to break these substrates down to ammonium. Urea utilization has been reported for marine ammonia-oxidizing communities7–10, but no evidence of cyanate utilization exists for marine ammonia oxidizers. Here, we demonstrate that in the Gulf of Mexico, Thaumarchaeota use urea and cyanate both directly and indirectly as energy and N sources. We observed substantial and linear rates of nitrite production from urea and cyanate additions, which often persisted even when ammonium was added to micromolar concentrations. Furthermore, single-cell analysis revealed that the Thaumarchaeota incorporated ammonium-, urea- and cyanate-derived N at significantly higher rates than most other microorganisms. Yet, no cyanases were detected in thaumarchaeal genomic data from the Gulf of Mexico. Therefore, we tested cyanate utilization in Nitrosopumilus maritimus, which also lacks a canonical cyanase, and showed that cyanate was oxidized to nitrite. Our findings demonstrate that marine Thaumarchaeota can use urea and cyanate as both an energy and N source. On the basis of these results, we hypothesize that urea and cyanate are substrates for ammonia-oxidizing Thaumarchaeota throughout the ocean.

Original languageEnglish
JournalNature Microbiology
Volume4
Issue number2
Pages (from-to)234-243
ISSN2058-5276
DOIs
Publication statusPublished - 2019

Fingerprint

Cyanates
Urea
Ammonium Compounds
Ammonia
Gulf of Mexico

Keywords

  • Ammonia/chemistry
  • Archaea/classification
  • Cyanates/chemistry
  • Energy Metabolism
  • Gulf of Mexico
  • Nitrification/physiology
  • Nitrites/metabolism
  • Oxidation-Reduction
  • Oxygen/analysis
  • Phylogeny
  • Seawater/chemistry
  • Urea/chemistry

Cite this

Kitzinger, K., Padilla, C. C., Marchant, H. K., Hach, P. F., Herbold, C. W., Kidane, A. T., ... Bristow, L. A. (2019). Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. Nature Microbiology, 4(2), 234-243. https://doi.org/10.1038/s41564-018-0316-2
Kitzinger, Katharina ; Padilla, Cory C. ; Marchant, Hannah K. ; Hach, Philipp F. ; Herbold, Craig W. ; Kidane, Abiel T. ; Könneke, Martin ; Littmann, Sten ; Mooshammer, Maria ; Niggemann, Jutta ; Petrov, Sandra ; Richter, Andreas ; Stewart, Frank J. ; Wagner, Michael ; Kuypers, Marcel M.M. ; Bristow, Laura A. / Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. In: Nature Microbiology. 2019 ; Vol. 4, No. 2. pp. 234-243.
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abstract = "Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant marine microorganisms1. These organisms thrive in the oceans despite ammonium being present at low nanomolar concentrations2,3. Some Thaumarchaeota isolates have been shown to utilize urea and cyanate as energy and N sources through intracellular conversion to ammonium4–6. Yet, it is unclear whether patterns observed in culture extend to marine Thaumarchaeota, and whether Thaumarchaeota in the ocean directly utilize urea and cyanate or rely on co-occurring microorganisms to break these substrates down to ammonium. Urea utilization has been reported for marine ammonia-oxidizing communities7–10, but no evidence of cyanate utilization exists for marine ammonia oxidizers. Here, we demonstrate that in the Gulf of Mexico, Thaumarchaeota use urea and cyanate both directly and indirectly as energy and N sources. We observed substantial and linear rates of nitrite production from urea and cyanate additions, which often persisted even when ammonium was added to micromolar concentrations. Furthermore, single-cell analysis revealed that the Thaumarchaeota incorporated ammonium-, urea- and cyanate-derived N at significantly higher rates than most other microorganisms. Yet, no cyanases were detected in thaumarchaeal genomic data from the Gulf of Mexico. Therefore, we tested cyanate utilization in Nitrosopumilus maritimus, which also lacks a canonical cyanase, and showed that cyanate was oxidized to nitrite. Our findings demonstrate that marine Thaumarchaeota can use urea and cyanate as both an energy and N source. On the basis of these results, we hypothesize that urea and cyanate are substrates for ammonia-oxidizing Thaumarchaeota throughout the ocean.",
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author = "Katharina Kitzinger and Padilla, {Cory C.} and Marchant, {Hannah K.} and Hach, {Philipp F.} and Herbold, {Craig W.} and Kidane, {Abiel T.} and Martin K{\"o}nneke and Sten Littmann and Maria Mooshammer and Jutta Niggemann and Sandra Petrov and Andreas Richter and Stewart, {Frank J.} and Michael Wagner and Kuypers, {Marcel M.M.} and Bristow, {Laura A.}",
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Kitzinger, K, Padilla, CC, Marchant, HK, Hach, PF, Herbold, CW, Kidane, AT, Könneke, M, Littmann, S, Mooshammer, M, Niggemann, J, Petrov, S, Richter, A, Stewart, FJ, Wagner, M, Kuypers, MMM & Bristow, LA 2019, 'Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment', Nature Microbiology, vol. 4, no. 2, pp. 234-243. https://doi.org/10.1038/s41564-018-0316-2

Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. / Kitzinger, Katharina; Padilla, Cory C.; Marchant, Hannah K.; Hach, Philipp F.; Herbold, Craig W.; Kidane, Abiel T.; Könneke, Martin; Littmann, Sten; Mooshammer, Maria; Niggemann, Jutta; Petrov, Sandra; Richter, Andreas; Stewart, Frank J.; Wagner, Michael; Kuypers, Marcel M.M.; Bristow, Laura A.

In: Nature Microbiology, Vol. 4, No. 2, 2019, p. 234-243.

Research output: Contribution to journalLetterResearchpeer-review

TY - JOUR

T1 - Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment

AU - Kitzinger, Katharina

AU - Padilla, Cory C.

AU - Marchant, Hannah K.

AU - Hach, Philipp F.

AU - Herbold, Craig W.

AU - Kidane, Abiel T.

AU - Könneke, Martin

AU - Littmann, Sten

AU - Mooshammer, Maria

AU - Niggemann, Jutta

AU - Petrov, Sandra

AU - Richter, Andreas

AU - Stewart, Frank J.

AU - Wagner, Michael

AU - Kuypers, Marcel M.M.

AU - Bristow, Laura A.

PY - 2019

Y1 - 2019

N2 - Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant marine microorganisms1. These organisms thrive in the oceans despite ammonium being present at low nanomolar concentrations2,3. Some Thaumarchaeota isolates have been shown to utilize urea and cyanate as energy and N sources through intracellular conversion to ammonium4–6. Yet, it is unclear whether patterns observed in culture extend to marine Thaumarchaeota, and whether Thaumarchaeota in the ocean directly utilize urea and cyanate or rely on co-occurring microorganisms to break these substrates down to ammonium. Urea utilization has been reported for marine ammonia-oxidizing communities7–10, but no evidence of cyanate utilization exists for marine ammonia oxidizers. Here, we demonstrate that in the Gulf of Mexico, Thaumarchaeota use urea and cyanate both directly and indirectly as energy and N sources. We observed substantial and linear rates of nitrite production from urea and cyanate additions, which often persisted even when ammonium was added to micromolar concentrations. Furthermore, single-cell analysis revealed that the Thaumarchaeota incorporated ammonium-, urea- and cyanate-derived N at significantly higher rates than most other microorganisms. Yet, no cyanases were detected in thaumarchaeal genomic data from the Gulf of Mexico. Therefore, we tested cyanate utilization in Nitrosopumilus maritimus, which also lacks a canonical cyanase, and showed that cyanate was oxidized to nitrite. Our findings demonstrate that marine Thaumarchaeota can use urea and cyanate as both an energy and N source. On the basis of these results, we hypothesize that urea and cyanate are substrates for ammonia-oxidizing Thaumarchaeota throughout the ocean.

AB - Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant marine microorganisms1. These organisms thrive in the oceans despite ammonium being present at low nanomolar concentrations2,3. Some Thaumarchaeota isolates have been shown to utilize urea and cyanate as energy and N sources through intracellular conversion to ammonium4–6. Yet, it is unclear whether patterns observed in culture extend to marine Thaumarchaeota, and whether Thaumarchaeota in the ocean directly utilize urea and cyanate or rely on co-occurring microorganisms to break these substrates down to ammonium. Urea utilization has been reported for marine ammonia-oxidizing communities7–10, but no evidence of cyanate utilization exists for marine ammonia oxidizers. Here, we demonstrate that in the Gulf of Mexico, Thaumarchaeota use urea and cyanate both directly and indirectly as energy and N sources. We observed substantial and linear rates of nitrite production from urea and cyanate additions, which often persisted even when ammonium was added to micromolar concentrations. Furthermore, single-cell analysis revealed that the Thaumarchaeota incorporated ammonium-, urea- and cyanate-derived N at significantly higher rates than most other microorganisms. Yet, no cyanases were detected in thaumarchaeal genomic data from the Gulf of Mexico. Therefore, we tested cyanate utilization in Nitrosopumilus maritimus, which also lacks a canonical cyanase, and showed that cyanate was oxidized to nitrite. Our findings demonstrate that marine Thaumarchaeota can use urea and cyanate as both an energy and N source. On the basis of these results, we hypothesize that urea and cyanate are substrates for ammonia-oxidizing Thaumarchaeota throughout the ocean.

KW - Ammonia/chemistry

KW - Archaea/classification

KW - Cyanates/chemistry

KW - Energy Metabolism

KW - Gulf of Mexico

KW - Nitrification/physiology

KW - Nitrites/metabolism

KW - Oxidation-Reduction

KW - Oxygen/analysis

KW - Phylogeny

KW - Seawater/chemistry

KW - Urea/chemistry

U2 - 10.1038/s41564-018-0316-2

DO - 10.1038/s41564-018-0316-2

M3 - Letter

C2 - 30531977

AN - SCOPUS:85058150127

VL - 4

SP - 234

EP - 243

JO - Nature Microbiology

JF - Nature Microbiology

SN - 2058-5276

IS - 2

ER -