Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic

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  • A Corrigendum to this article was published on 22 January 2009

Abstract

Aerobic nitrification of ammonia to nitrite and nitrate is a key process in the oceanic nitrogen cycling mediated by prokaryotes1. Apart from Bacteria belonging to the β- and γ-Proteobacteria involved in the first nitrification step, Crenarchaeota have recently been recognized as main drivers of the oxidation of ammonia to nitrite in soil as well as in the ocean, as indicated by the dominance of archaeal ammonia monooxygenase (amoA) genes over bacterial amoA2,3. Evidence is accumulating that archaeal amoA genes are common in a wide range of marine systems3,4,5,6. Essentially, all these reports focused on surface and mesopelagic (200–1,000 m depth) waters, where ammonia concentrations are higher than in waters below 1,000 m depth. However, Crenarchaeota are also abundant in the water column below 1,000 m, where ammonia concentrations are extremely low. Here we show that, throughout the North Atlantic Ocean, the abundance of archaeal amoA genes decreases markedly from subsurface waters to 4,000 m depth, and from subpolar to equatorial deep waters, leading to pronounced vertical and latitudinal gradients in the ratio of archaeal amoA to crenarchaeal 16S ribosomal RNA (rRNA) genes. The lack of significant copy numbers of amoA genes and the very low fixation rates of dark carbon dioxide in the bathypelagic North Atlantic suggest that most bathypelagic Crenarchaeota are not autotrophic ammonia oxidizers: most likely, they utilize organic matter and hence live heterotrophically.

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Figure 1: Latitudinal and depth distribution of crenarchaeal 16S rRNA and archaeal amoA copy numbers in the eastern North Atlantic.
Figure 2: Phylogenetic tree of archaeal amoA sequences recovered from the North Atlantic.
Figure 3: Archaeal amoA copy numbers versus CO 2 fixation.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The archaeal sequences are deposited in GenBank under accession numbers EU650236EU650270 (station 3, ARCHIMEDES-2), FJ002858FJ002876 (station 23, ARCHIMEDES-3), FJ150794FJ150834 (Station 9, TRANSAT-1) for 16S rRNA genes and EU795424EU795460 and EU810209EU810235 for amoA genes.

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Acknowledgements

We thank the captain and crew of the RV Pelagia for their help during work at sea. We thank H. M. van Aken for the characterization of the water masses, J. M. Arrieta for collecting the samples during the TRANSAT-1 cruise, B. Abbas, J. van Bleijswijk and H. Witte for technical discussions about the qPCR and phylogenetic analyses, and T. Reinthaler for discussions. We also thank A. Hunting, A. M. Schmitz and W. D. Lienhart for help with data processing. This research was supported by a Marie Curie Fellowship of the European Community to H.A. Shiptime was provided through grants of the Earth and Life Science Division of the Dutch Science Foundation (ALW-NWO) (TRANSAT and ARCHIMEDES projects) to G.J.H. The work was performed within the frame of the ‘Networks of Excellence’ MarBef and EurOceans supported by the 6th Framework Program of the European Union.

Author Contributions The manuscript was written by H.A. and G.J.H. DNA extractions were performed by H.A. and M.B., qPCR by H.A., M.B. and J.D. and phylogenetic analyses by M.B. Measurements of dissolved inorganic carbon incorporation were done by G.J.H.

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Correspondence to Gerhard J. Herndl.

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This file contains Supplementary Methods, a Supplementary Discussion, Supplementary Tables S1-S4, Supplementary Figures S1-S5 with legends and additional references. (PDF 1537 kb)

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Agogué, H., Brink, M., Dinasquet, J. et al. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456, 788–791 (2008) doi:10.1038/nature07535

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