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

• Published in: Nature microbiology Vol. 4; no. 2; pp. 234 - 243
• Main Authors: 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.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01-02-2019; Nature Publishing Group
• Subjects: 14/32; 45/23; 45/91; 631/326/171/1878; 631/326/26; Ammonia; Ammonia - chemistry; Ammonia - metabolism; Ammonium; Archaea - classification; Archaea - genetics; Archaea - metabolism; Biomedical and Life Sciences; Cell culture; Cyanates - chemistry; Cyanates - metabolism; Energy; Energy Metabolism; Gulf of Mexico; Infectious Diseases; Letter; Life Sciences; Marine environment; Medical Microbiology; Microbiology; Microorganisms; Nitrates; Nitrification; Nitrification - physiology; Nitrites - metabolism; Oceans; Oxidation-Reduction; Oxygen - analysis; Parasitology; Phylogeny; Seawater - chemistry; Seawater - microbiology; Thaumarchaeota; Urea; Urea - chemistry; Urea - metabolism; Virology; Gulf of Mexico
• ISSN: 2058-5276; 2058-5276
• DOI: 10.1038/s41564-018-0316-2

Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant marine microorganisms
1
. These organisms thrive in the oceans despite ammonium being present at low nanomolar concentrations
2
,
3
. Some Thaumarchaeota isolates have been shown to utilize urea and cyanate as energy and N sources through intracellular conversion to ammonium
4
–
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 communities
7
–
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.
Thaumarchaeota isolates are capable of utilizing urea and cyanate for nitrification in vitro. Here, the authors show that this occurs in situ and that Thaumarchaeota are able to use urea and cyanate as an energy and nitrogen source in the marine environment.