Oxygen and nitrogen production by an ammonia-oxidizing archaeon
Consuming oxygen, but making it too
For marine microbes, there are myriad biological reactions involved in the cycling of nutrients and the generation of energy. Availability of oxygen is crucial for many species’ metabolism. Kraft et al. were surprised to find that pure cultures of an ammonia-oxidizing archaean (AOA) (see the Perspective by Martens-Habbena and Qin), Nitosopumilus maritimus, were able to regenerate small amounts of oxygen when placed under anoxic conditions. Isotope labeling of nitrogen species revealed a series of reactions transforming nitrite, the expected metabolic end product, into nitric oxide, nitrous oxide, and, eventually, dinitrogen. Oxygen was also formed, likely from nitric oxide disproportionation, but was mostly consumed, which is consistent with the overall aerobic metabolism of AOA. These organisms can be found in oxygen-depleted waters and may benefit from producing oxygen from nitrite under these conditions. —MAF
Abstract
Ammonia-oxidizing archaea (AOA) are one of the most abundant groups of microbes in the world’s oceans and are key players in the nitrogen cycle. Their energy metabolism—the oxidation of ammonia to nitrite—requires oxygen. Nevertheless, AOA are abundant in environments where oxygen is undetectable. By carrying out incubations for which oxygen concentrations were resolved to the nanomolar range, we show that after oxygen depletion, Nitrosopumilus maritimus produces dinitrogen and oxygen, which is used for ammonia oxidation. The pathway is not completely resolved but likely has nitric oxide and nitrous oxide as key intermediates. N. maritimus joins a handful of organisms known to produce oxygen in the dark. On the basis of this ability, we reevaluate the role of N. maritimus in oxygen-depleted marine environments.
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Science
Volume 375 | Issue 6576
7 January 2022
7 January 2022
Copyright
Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
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Submission history
Received: 21 November 2020
Accepted: 28 October 2021
Published in print: 7 January 2022
Acknowledgments
We thank A. Glud for assistance with microelectrode measurements and providing microelectrodes. D.E.C. is a Villum investigator.
Funding: This work was supported by the Villum Foundation, Denmark (Villum Young Investigator Grant 25491 to B.K. and Villum Investigator Grant 16518 to D.E.C.); the Independent Research Fund Denmark (grant 14181-00025 to D.E.C.); and the Heisenberg Program of the Deutsche Forschungsgemeinschaft awarded (KO 3651/6-1) to M.K.
Author contributions: B.K. and D.E.C. designed the experiments. B.K. performed the experiments and analyzed data with input from M.L., L.A.B., M.K., B.T., and D.E.C. B.K. and D.E.C. wrote the manuscript, with contributions and approval from all other authors.
Competing interests: The authors declare no conflicts of interest.
Data and materials availability: All data are available in the main text or the supplementary materials.
Authors
Funding Information
Natur og Univers, Det Frie Forskningsråd: 14181-00025
Villum Fonden: 25491
Villum Fonden: 16518
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