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The metagenome of the marine anammox bacterium ‘Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium

The metagenome of the marine anammox bacterium ‘Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium
The metagenome of the marine anammox bacterium ‘Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium
Anaerobic ammonium-oxidizing (anammox) bacteria are responsible for a significant portion of the loss of fixed nitrogen from the oceans, making them important players in the global nitrogen cycle. To date, marine anammox bacteria found in marine water columns and sediments worldwide belong almost exclusively to the 'Candidatus Scalindua' species, but the molecular basis of their metabolism and competitive fitness is presently unknown. We applied community sequencing of a marine anammox enrichment culture dominated by 'Candidatus Scalindua profunda' to construct a genome assembly, which was subsequently used to analyse the most abundant gene transcripts and proteins. In the S. profunda assembly, 4756 genes were annotated, and only about half of them showed the highest identity to the only other anammox bacterium of which a metagenome assembly had been constructed so far, the freshwater 'Candidatus Kuenenia stuttgartiensis'. In total, 2016 genes of S. profunda could not be matched to the K. stuttgartiensis metagenome assembly at all, and a similar number of genes in K. stuttgartiensis could not be found in S. profunda. Most of these genes did not have a known function but 98 expressed genes could be attributed to oligopeptide transport, amino acid metabolism, use of organic acids and electron transport. On the basis of the S. profunda metagenome, and environmental metagenome data, we observed pronounced differences in the gene organization and expression of important anammox enzymes, such as hydrazine synthase (HzsAB), nitrite reductase (NirS) and inorganic nitrogen transport proteins. Adaptations of Scalindua to the substrate limitation of the ocean may include highly expressed ammonium, nitrite and oligopeptide transport systems and pathways for the transport, oxidation, and assimilation of small organic compounds that may allow a more versatile lifestyle contributing to the competitive fitness of Scalindua in the marine realm.
1462-2920
1275-1289
van de Vossenberg, Jack
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Woebken, Dagmar
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Maalcke, Wouter J.
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Wessels, Hans J.C.T.
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Dutilh, Bas E.
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Kartal, Boran
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Janssen-Megens, Eva M.
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Roeselers, Guus
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Yan, Jia
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Speth, Daan
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Gloerich, Jolein
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Geerts, Wim
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van der Biezen, Erwin
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Pluk, Wendy
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Francoijs, Kees-Jan
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Russ, Lina
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Lam, Phyllis
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Malfatti, Stefanie A.
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Tringe, Susannah Green
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Haaijer, Suzanne C.M.
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Op den Camp, Huub J.M.
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Stunnenberg, Henk G.
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Amann, Rudi
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Kuypers, Marcel M.M.
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Jetten, Mike S.M.
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van de Vossenberg, Jack
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Woebken, Dagmar
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Maalcke, Wouter J.
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Dutilh, Bas E.
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Kartal, Boran
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Janssen-Megens, Eva M.
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Roeselers, Guus
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Yan, Jia
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Speth, Daan
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Gloerich, Jolein
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Geerts, Wim
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van der Biezen, Erwin
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Pluk, Wendy
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Francoijs, Kees-Jan
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Russ, Lina
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Lam, Phyllis
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Malfatti, Stefanie A.
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Tringe, Susannah Green
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Haaijer, Suzanne C.M.
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Op den Camp, Huub J.M.
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Stunnenberg, Henk G.
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Amann, Rudi
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Kuypers, Marcel M.M.
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Jetten, Mike S.M.
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van de Vossenberg, Jack, Woebken, Dagmar, Maalcke, Wouter J., Wessels, Hans J.C.T., Dutilh, Bas E., Kartal, Boran, Janssen-Megens, Eva M., Roeselers, Guus, Yan, Jia, Speth, Daan, Gloerich, Jolein, Geerts, Wim, van der Biezen, Erwin, Pluk, Wendy, Francoijs, Kees-Jan, Russ, Lina, Lam, Phyllis, Malfatti, Stefanie A., Tringe, Susannah Green, Haaijer, Suzanne C.M., Op den Camp, Huub J.M., Stunnenberg, Henk G., Amann, Rudi, Kuypers, Marcel M.M. and Jetten, Mike S.M. (2013) The metagenome of the marine anammox bacterium ‘Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium. Environmental Microbiology, 15 (5), 1275-1289. (doi:10.1111/j.1462-2920.2012.02774.x). (PMID:22568606)

Record type: Article

Abstract

Anaerobic ammonium-oxidizing (anammox) bacteria are responsible for a significant portion of the loss of fixed nitrogen from the oceans, making them important players in the global nitrogen cycle. To date, marine anammox bacteria found in marine water columns and sediments worldwide belong almost exclusively to the 'Candidatus Scalindua' species, but the molecular basis of their metabolism and competitive fitness is presently unknown. We applied community sequencing of a marine anammox enrichment culture dominated by 'Candidatus Scalindua profunda' to construct a genome assembly, which was subsequently used to analyse the most abundant gene transcripts and proteins. In the S. profunda assembly, 4756 genes were annotated, and only about half of them showed the highest identity to the only other anammox bacterium of which a metagenome assembly had been constructed so far, the freshwater 'Candidatus Kuenenia stuttgartiensis'. In total, 2016 genes of S. profunda could not be matched to the K. stuttgartiensis metagenome assembly at all, and a similar number of genes in K. stuttgartiensis could not be found in S. profunda. Most of these genes did not have a known function but 98 expressed genes could be attributed to oligopeptide transport, amino acid metabolism, use of organic acids and electron transport. On the basis of the S. profunda metagenome, and environmental metagenome data, we observed pronounced differences in the gene organization and expression of important anammox enzymes, such as hydrazine synthase (HzsAB), nitrite reductase (NirS) and inorganic nitrogen transport proteins. Adaptations of Scalindua to the substrate limitation of the ocean may include highly expressed ammonium, nitrite and oligopeptide transport systems and pathways for the transport, oxidation, and assimilation of small organic compounds that may allow a more versatile lifestyle contributing to the competitive fitness of Scalindua in the marine realm.

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More information

e-pub ahead of print date: 9 May 2012
Published date: May 2013
Organisations: Ocean Biochemistry & Ecosystems

Identifiers

Local EPrints ID: 349911
URI: http://eprints.soton.ac.uk/id/eprint/349911
ISSN: 1462-2920
PURE UUID: e44338c5-195d-41aa-bb5f-6fc1219386e3
ORCID for Phyllis Lam: ORCID iD orcid.org/0000-0003-2067-171X

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Date deposited: 13 Mar 2013 13:30
Last modified: 15 Mar 2024 03:47

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Contributors

Author: Jack van de Vossenberg
Author: Dagmar Woebken
Author: Wouter J. Maalcke
Author: Hans J.C.T. Wessels
Author: Bas E. Dutilh
Author: Boran Kartal
Author: Eva M. Janssen-Megens
Author: Guus Roeselers
Author: Jia Yan
Author: Daan Speth
Author: Jolein Gloerich
Author: Wim Geerts
Author: Erwin van der Biezen
Author: Wendy Pluk
Author: Kees-Jan Francoijs
Author: Lina Russ
Author: Phyllis Lam ORCID iD
Author: Stefanie A. Malfatti
Author: Susannah Green Tringe
Author: Suzanne C.M. Haaijer
Author: Huub J.M. Op den Camp
Author: Henk G. Stunnenberg
Author: Rudi Amann
Author: Marcel M.M. Kuypers
Author: Mike S.M. Jetten

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