Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria

Sangita Ganesh, Anthony D. Bertagnolli, Laura A. Bristow, Cory C. Padilla, Nigel Blackwood, Montserrat Aldunate, Annie Bourbonnais, Mark A. Altabet, Rex R. Malmstrom, Tanja Woyke, Osvaldo Ulloa, Konstantinos T. Konstantinidis, Bo Thamdrup, Frank J. Stewart

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Abstract

Anaerobic ammonium oxidation (anammox) contributes substantially to ocean nitrogen loss, particularly in anoxic marine zones (AMZs). Ammonium is scarce in AMZs, raising the hypothesis that organic nitrogen compounds may be ammonium sources for anammox. Biochemical measurements suggest that the organic compounds urea and cyanate can support anammox in AMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonium themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria, and genomic evidence for cyanate use for anammox is limited to a cyanase gene recovered from the sediment bacterium Candidatus Scalindua profunda. Here, analysis of Ca. Scalindua single amplified genomes from the Eastern Tropical North Pacific AMZ revealed genes for urea degradation and transport, as well as for cyanate degradation. Urease and cyanase genes were transcribed, along with anammox genes, in the AMZ core where anammox rates peaked. Homologs of these genes were also detected in meta-omic datasets from major AMZs in the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from different ocean regions can directly access organic nitrogen substrates. Future studies should assess if and under what environmental conditions these substrates contribute to the ammonium budget for anammox.
Original languageEnglish
JournalI S M E Journal
Volume12
Pages (from-to)2706–2722
ISSN1751-7362
DOIs
Publication statusPublished - 1. Nov 2018

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transcriptomics
Ammonium Compounds
genomics
Nitrogen
ammonium
oxidation
substrate
bacterium
nitrogen
bacteria
cyanates
cells
Cyanates
gene
genes
urea
Urea
degradation
Military Personnel
organic nitrogen compounds

Keywords

  • Ammonium Compounds/metabolism
  • Anaerobiosis
  • Bacteria/genetics
  • Carbon-Nitrogen Lyases/genetics
  • Gene Expression Profiling
  • Genomics
  • Nitrogen/metabolism
  • Oceans and Seas
  • Oxidation-Reduction
  • Seawater/microbiology
  • Single-Cell Analysis
  • Urease/genetics

Cite this

Ganesh, S., Bertagnolli, A. D., Bristow, L. A., Padilla, C. C., Blackwood, N., Aldunate, M., ... Stewart, F. J. (2018). Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria. I S M E Journal, 12, 2706–2722. https://doi.org/10.1038/s41396-018-0223-9
Ganesh, Sangita ; Bertagnolli, Anthony D. ; Bristow, Laura A. ; Padilla, Cory C. ; Blackwood, Nigel ; Aldunate, Montserrat ; Bourbonnais, Annie ; Altabet, Mark A. ; Malmstrom, Rex R. ; Woyke, Tanja ; Ulloa, Osvaldo ; Konstantinidis, Konstantinos T. ; Thamdrup, Bo ; Stewart, Frank J. / Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria. In: I S M E Journal. 2018 ; Vol. 12. pp. 2706–2722.
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abstract = "Anaerobic ammonium oxidation (anammox) contributes substantially to ocean nitrogen loss, particularly in anoxic marine zones (AMZs). Ammonium is scarce in AMZs, raising the hypothesis that organic nitrogen compounds may be ammonium sources for anammox. Biochemical measurements suggest that the organic compounds urea and cyanate can support anammox in AMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonium themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria, and genomic evidence for cyanate use for anammox is limited to a cyanase gene recovered from the sediment bacterium Candidatus Scalindua profunda. Here, analysis of Ca. Scalindua single amplified genomes from the Eastern Tropical North Pacific AMZ revealed genes for urea degradation and transport, as well as for cyanate degradation. Urease and cyanase genes were transcribed, along with anammox genes, in the AMZ core where anammox rates peaked. Homologs of these genes were also detected in meta-omic datasets from major AMZs in the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from different ocean regions can directly access organic nitrogen substrates. Future studies should assess if and under what environmental conditions these substrates contribute to the ammonium budget for anammox.",
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author = "Sangita Ganesh and Bertagnolli, {Anthony D.} and Bristow, {Laura A.} and Padilla, {Cory C.} and Nigel Blackwood and Montserrat Aldunate and Annie Bourbonnais and Altabet, {Mark A.} and Malmstrom, {Rex R.} and Tanja Woyke and Osvaldo Ulloa and Konstantinidis, {Konstantinos T.} and Bo Thamdrup and Stewart, {Frank J.}",
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Ganesh, S, Bertagnolli, AD, Bristow, LA, Padilla, CC, Blackwood, N, Aldunate, M, Bourbonnais, A, Altabet, MA, Malmstrom, RR, Woyke, T, Ulloa, O, Konstantinidis, KT, Thamdrup, B & Stewart, FJ 2018, 'Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria', I S M E Journal, vol. 12, pp. 2706–2722. https://doi.org/10.1038/s41396-018-0223-9

Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria. / Ganesh, Sangita; Bertagnolli, Anthony D.; Bristow, Laura A.; Padilla, Cory C.; Blackwood, Nigel; Aldunate, Montserrat; Bourbonnais, Annie; Altabet, Mark A.; Malmstrom, Rex R.; Woyke, Tanja; Ulloa, Osvaldo; Konstantinidis, Konstantinos T.; Thamdrup, Bo; Stewart, Frank J.

In: I S M E Journal, Vol. 12, 01.11.2018, p. 2706–2722.

Research output: Contribution to journalJournal articleResearchpeer-review

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T1 - Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria

AU - Ganesh, Sangita

AU - Bertagnolli, Anthony D.

AU - Bristow, Laura A.

AU - Padilla, Cory C.

AU - Blackwood, Nigel

AU - Aldunate, Montserrat

AU - Bourbonnais, Annie

AU - Altabet, Mark A.

AU - Malmstrom, Rex R.

AU - Woyke, Tanja

AU - Ulloa, Osvaldo

AU - Konstantinidis, Konstantinos T.

AU - Thamdrup, Bo

AU - Stewart, Frank J.

PY - 2018/11/1

Y1 - 2018/11/1

N2 - Anaerobic ammonium oxidation (anammox) contributes substantially to ocean nitrogen loss, particularly in anoxic marine zones (AMZs). Ammonium is scarce in AMZs, raising the hypothesis that organic nitrogen compounds may be ammonium sources for anammox. Biochemical measurements suggest that the organic compounds urea and cyanate can support anammox in AMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonium themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria, and genomic evidence for cyanate use for anammox is limited to a cyanase gene recovered from the sediment bacterium Candidatus Scalindua profunda. Here, analysis of Ca. Scalindua single amplified genomes from the Eastern Tropical North Pacific AMZ revealed genes for urea degradation and transport, as well as for cyanate degradation. Urease and cyanase genes were transcribed, along with anammox genes, in the AMZ core where anammox rates peaked. Homologs of these genes were also detected in meta-omic datasets from major AMZs in the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from different ocean regions can directly access organic nitrogen substrates. Future studies should assess if and under what environmental conditions these substrates contribute to the ammonium budget for anammox.

AB - Anaerobic ammonium oxidation (anammox) contributes substantially to ocean nitrogen loss, particularly in anoxic marine zones (AMZs). Ammonium is scarce in AMZs, raising the hypothesis that organic nitrogen compounds may be ammonium sources for anammox. Biochemical measurements suggest that the organic compounds urea and cyanate can support anammox in AMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonium themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria, and genomic evidence for cyanate use for anammox is limited to a cyanase gene recovered from the sediment bacterium Candidatus Scalindua profunda. Here, analysis of Ca. Scalindua single amplified genomes from the Eastern Tropical North Pacific AMZ revealed genes for urea degradation and transport, as well as for cyanate degradation. Urease and cyanase genes were transcribed, along with anammox genes, in the AMZ core where anammox rates peaked. Homologs of these genes were also detected in meta-omic datasets from major AMZs in the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from different ocean regions can directly access organic nitrogen substrates. Future studies should assess if and under what environmental conditions these substrates contribute to the ammonium budget for anammox.

KW - Ammonium Compounds/metabolism

KW - Anaerobiosis

KW - Bacteria/genetics

KW - Carbon-Nitrogen Lyases/genetics

KW - Gene Expression Profiling

KW - Genomics

KW - Nitrogen/metabolism

KW - Oceans and Seas

KW - Oxidation-Reduction

KW - Seawater/microbiology

KW - Single-Cell Analysis

KW - Urease/genetics

U2 - 10.1038/s41396-018-0223-9

DO - 10.1038/s41396-018-0223-9

M3 - Journal article

C2 - 29991764

VL - 12

SP - 2706

EP - 2722

JO - I S M E Journal

JF - I S M E Journal

SN - 1751-7362

ER -