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

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 ammonium4,5,6. 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 communities7,8,9,10, 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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Fig. 1: Depth distribution of nutrient and oxygen concentrations, Thaumarchaeota cell counts and oxidation rates from Station 2.
Fig. 2: Production of 15N-nitrite over time and correlations between rates obtained from various substrate additions.
Fig. 3: Thaumarchaeota single-cell ammonium, urea and cyanate uptake determined by nanoSIMS at Station 2, 14 m depth.
Fig. 4: amoA-based phylogeny of Thaumarchaeota MAGs recovered in this study and cyanate utilization by the marine thaumarchaeon N. maritimus.

Data availability

All sequence data and thaumarchaeal MAGs generated in this study are deposited in NCBI under BioProject number: PRJNA397176. Metatranscriptomes are deposited under BioSample numbers SAMN07461123SAMN07461125; 16S amplicon sequencing under SAMN07461114SAMN07461122; metagenomes under SAMN10227777SAMN10227781 and MAGs under SAMN10233969SAMN10233974. Accession numbers of sequences used for tree calculations (16S rRNA gene, amoA, UreC, CynS, and genome sequences) are given in Supplementary Table 9. CTD data, measured nutrient concentrations, process rates, Thaumarchaeota relative abundance based on 16S rRNA gene amplicon sequencing and Thaumarchaeota-specific CARD-FISH counts are given in Supplementary Table 10.

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Acknowledgements

The authors thank the captain and crew of the R/V Pelican PE17-02 cruise. The authors are grateful to G. Klockgether, D. Tienken, I. Ulber, L. Seidl, W. Neweshy, N. Alrubeay, M. Philippi and D. J. Parris for technical support; G. Lavik, J. Milucka, W. Mohr, N. Lehnen and S. Ahmerkamp for fruitful discussions. This research was funded by the Max-Planck-Society, the European Research Council Advanced Grant project NITRICARE 294343 (to M.W.) and the National Science Foundation grants 1558916 and 1564559 (to F.J.S.)

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L.A.B., K.K., H.K.M., M.M.M.K. and M.W. designed the study. K.K., L.A.B. and H.K.M. performed experiments, S.L. and A.T.K. ran nanoSIMS analyses. K.K., L.A.B., H.K.M. and P.F.H. analysed samples and data. C.C.P. sampled for and performed molecular analyses with contribution from C.W.H. and F.J.S. Cyanate concentrations were measured by M.M. and A.R.; total dissolved nitrogen was analysed by J.N. Cultures were provided by S.P. and M.K. The manuscript was written by K.K., L.A.B. and H.K.M., with contributions from all co-authors.

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Correspondence to Hannah K. Marchant.

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Reporting Summary

Supplementary Table 1

Statistics for rate calculations at all stations and depths (one-tailed t-test).

Supplementary Table 9

Accession numbers of sequences used for 16S rRNA gene tree, amoA, CynS, UreC and genome trees.

Supplementary Table 10

CTD data, measured nutrient concentrations, process rates, relative abundance of Thaumarchaeota based on 16S rRNA gene amplicon sequencing and Thaumarchaeota-specific CARD-FISH counts.

Supplementary File 1

UreC tree with bootstrap values (PDF).

Supplementary File 2

UreC tree with bootstrap values (tree).

Supplementary File 3

UreC tree with node labels (PDF).

Supplementary File 4

UreC tree with node labels (tree).

Supplementary File 5

UreC tree annotation.

Supplementary File 6

Read-fragment-mapping UreC.

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Kitzinger, K., Padilla, C.C., Marchant, H.K. et al. Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. Nat Microbiol 4, 234–243 (2019). https://doi.org/10.1038/s41564-018-0316-2

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