Complete nitrification by Nitrospira bacteria

Holger Daims; Elena V. Lebedeva; Petra Pjevac; Ping Han; Craig Herbold; Mads Albertsen; Nico Jehmlich; Marton Palatinszky; Julia Vierheilig; Alexandr Bulaev; Rasmus H. Kirkegaard; Martin Von Bergen; Thomas Rattei; Bernd Bendinger; Per H. Nielsen; Michael Wagner

doi:10.1038/nature16461

Complete nitrification by Nitrospira bacteria

Holger Daims
, Elena V. Lebedeva
, Petra Pjevac
, Ping Han
, Craig Herbold
, Mads Albertsen
, Nico Jehmlich
, Marton Palatinszky
, Julia Vierheilig
, Alexandr Bulaev
, Rasmus H. Kirkegaard
, Martin Von Bergen
, Thomas Rattei
, Bernd Bendinger
, Per H. Nielsen
, Michael Wagner

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

2412 Citations (Scopus)

Abstract

Nitrification, the oxidation of ammonia via nitrite to nitrate, has always been considered to be a two-step process catalysed by chemolithoautotrophic microorganisms oxidizing either ammonia or nitrite. No known nitrifier carries out both steps, although complete nitrification should be energetically advantageous. This functional separation has puzzled microbiologists for a century. Here we report on the discovery and cultivation of a completely nitrifying bacterium from the genus Nitrospira, a globally distributed group of nitrite oxidizers. The genome of this chemolithoautotrophic organism encodes the pathways both for ammonia and nitrite oxidation, which are concomitantly activated during growth by ammonia oxidation to nitrate. Genes affiliated with the phylogenetically distinct ammonia monooxygenase and hydroxylamine dehydrogenase genes of Nitrospira are present in many environments and were retrieved on Nitrospira-contigs in new metagenomes from engineered systems. These findings fundamentally change our picture of nitrification and point to completely nitrifying Nitrospira as key components of nitrogen-cycling microbial communities. © 2015 Macmillan Publishers Limited. All rights reserved.

Original language	English
Pages (from-to)	504-509
Journal	Nature
Volume	528
Issue number	7583
DOIs	https://doi.org/10.1038/nature16461
Publication status	Published - 24 Dec 2015
Externally published	Yes

Bibliographical note

Publication details (e.g. title, author(s), publication statuses and dates) are captured on an “AS IS” and “AS AVAILABLE” basis at the time of record harvesting from the data source. Suggestions for further amendments or supplementary information can be sent to [email protected].

Funding

Acknowledgements We thank T. K. Lee and M. Steinberger for help with PCR analyses, N. V. Grigor\u2019eva and M. Pogoda for assistance with culture maintenance, N. A. Kostrikina for assistance with electron microscopy, K. Kitzinger for support with FISH analyses, M. Mooshammer for help with chemical analyses, R. Hatzenpichler for designing probe Nmir1009, K. Eismann for help with proteome sample preparation, B. Scheer for help with mass spectrometer maintenance, Purena GmbH (Wolfenb\u00FCttel, Germany) for cooperation, N. Chernyh and J. Rosenthal for taking samples, and H. Koch and E. Bock for discussion. The authors are grateful for using the analytical facilities of the Centre for Chemical Microscopy (ProVIS) (Helmholtz Centre for Environmental Research), which is headed by H. Richnow (Department of Isotope Biochemistry) and supported by European Regional Development Funds (EFRE\u2013Europe funds Saxony) and the Helmholtz Association. P.P. and H.D. were supported by the Austrian Science Fund (FWF) projects P27319-B21 and P25231-B21 (to H.D.). M.P., J.V., P.H., and M.W. were supported by the European Research Council Advanced Grant project NITRICARE 294343 (to M.W.). M.A., R.H.K., and P.H.N. were supported by the Danish Council for Independent Research, DFF \u2013 4005-00369 and Innovation Fund Denmark (EcoDesign).

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abstract = "Nitrification, the oxidation of ammonia via nitrite to nitrate, has always been considered to be a two-step process catalysed by chemolithoautotrophic microorganisms oxidizing either ammonia or nitrite. No known nitrifier carries out both steps, although complete nitrification should be energetically advantageous. This functional separation has puzzled microbiologists for a century. Here we report on the discovery and cultivation of a completely nitrifying bacterium from the genus Nitrospira, a globally distributed group of nitrite oxidizers. The genome of this chemolithoautotrophic organism encodes the pathways both for ammonia and nitrite oxidation, which are concomitantly activated during growth by ammonia oxidation to nitrate. Genes affiliated with the phylogenetically distinct ammonia monooxygenase and hydroxylamine dehydrogenase genes of Nitrospira are present in many environments and were retrieved on Nitrospira-contigs in new metagenomes from engineered systems. These findings fundamentally change our picture of nitrification and point to completely nitrifying Nitrospira as key components of nitrogen-cycling microbial communities. {\textcopyright} 2015 Macmillan Publishers Limited. All rights reserved.",

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AU - Albertsen, Mads

AU - Jehmlich, Nico

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N2 - Nitrification, the oxidation of ammonia via nitrite to nitrate, has always been considered to be a two-step process catalysed by chemolithoautotrophic microorganisms oxidizing either ammonia or nitrite. No known nitrifier carries out both steps, although complete nitrification should be energetically advantageous. This functional separation has puzzled microbiologists for a century. Here we report on the discovery and cultivation of a completely nitrifying bacterium from the genus Nitrospira, a globally distributed group of nitrite oxidizers. The genome of this chemolithoautotrophic organism encodes the pathways both for ammonia and nitrite oxidation, which are concomitantly activated during growth by ammonia oxidation to nitrate. Genes affiliated with the phylogenetically distinct ammonia monooxygenase and hydroxylamine dehydrogenase genes of Nitrospira are present in many environments and were retrieved on Nitrospira-contigs in new metagenomes from engineered systems. These findings fundamentally change our picture of nitrification and point to completely nitrifying Nitrospira as key components of nitrogen-cycling microbial communities. © 2015 Macmillan Publishers Limited. All rights reserved.

AB - Nitrification, the oxidation of ammonia via nitrite to nitrate, has always been considered to be a two-step process catalysed by chemolithoautotrophic microorganisms oxidizing either ammonia or nitrite. No known nitrifier carries out both steps, although complete nitrification should be energetically advantageous. This functional separation has puzzled microbiologists for a century. Here we report on the discovery and cultivation of a completely nitrifying bacterium from the genus Nitrospira, a globally distributed group of nitrite oxidizers. The genome of this chemolithoautotrophic organism encodes the pathways both for ammonia and nitrite oxidation, which are concomitantly activated during growth by ammonia oxidation to nitrate. Genes affiliated with the phylogenetically distinct ammonia monooxygenase and hydroxylamine dehydrogenase genes of Nitrospira are present in many environments and were retrieved on Nitrospira-contigs in new metagenomes from engineered systems. These findings fundamentally change our picture of nitrification and point to completely nitrifying Nitrospira as key components of nitrogen-cycling microbial communities. © 2015 Macmillan Publishers Limited. All rights reserved.

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Complete nitrification by Nitrospira bacteria

Abstract

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