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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Accession codes
Primary accessions
GenBank/EMBL/DDBJ
Data deposits
The archaeal sequences are deposited in GenBank under accession numbers EU650236–EU650270 (station 3, ARCHIMEDES-2), FJ002858–FJ002876 (station 23, ARCHIMEDES-3), FJ150794–FJ150834 (Station 9, TRANSAT-1) for 16S rRNA genes and EU795424–EU795460 and EU810209–EU810235 for amoA genes.
References
Ward, B. B., Capone, D. G. & Zehr, J. P. What’s new in the nitrogen cycle? Oceanography 20, 101–109 (2007)
Schleper, C., Jurgens, G. & Jonuscheit, M. Genomic studies of uncultivated Archaea. Nature Rev. Microbiol. 3, 479–488 (2005)
Wuchter, C. et al. Archaeal nitrification in the ocean. Proc. Natl Acad. Sci. USA 103, 12317–12322 (2006)
Mincer, T. J. et al. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9, 1162–1175 (2007)
Beman, J. M., Popp, B. N. & Francis, C. A. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J. 2, 429–441 (2008)
Caffrey, J. M., Bano, N., Kalanetra, K. & Hollibaugh, J. T. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J. 1, 660–662 (2007)
Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001)
Herndl, G. J. et al. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl. Environ. Microbiol. 71, 2303–2309 (2005)
Church, M. J. et al. Abundance and distribution of planktonic Archaea and Bacteria in the waters west of the Antarctic Peninsula. Limnol. Oceanogr. 48, 1893–1902 (2003)
Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004)
Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E. & Oakley, B. B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl Acad. Sci. USA 102, 14683–14688 (2005)
Konneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005)
Hallam, S. J. et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl Acad. Sci. USA 103, 18296–18301 (2006)
Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809 (2006)
Nakagawa, T., Mori, K., Kato, C., Takahashi, R. & Tokuyama, T. Distribution of the cold-adapted ammonia-oxidizing microorganisms in the deep-ocean of the northeastern Japan Sea. Microbes Environ. 22, 365–372 (2007)
Ouverney, C. C. & Fuhrman, J. A. Marine planktonic Archaea take up amino acids. Appl. Environ. Microbiol. 66, 4829–4833 (2000)
Teira, E., van Aken, H., Veth, C. & Herndl, G. J. Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnol. Oceanogr. 51, 60–69 (2006)
Kirchman, D. L., Elifantz, H., Dittel, A. I., Malmstrom, R. R. & Cottrell, M. T. Standing stocks and activity of Archaea and Bacteria in the western Arctic Ocean. Limnol. Oceanogr. 52, 495–507 (2007)
Ingalls, A. E. et al. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Natl Acad. Sci. USA 103, 6442–6447 (2006)
Teira, E., Lebaron, P., van Aken, H. & Herndl, G. J. Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnol. Oceanogr. 51, 2131–2144 (2006)
Varela, M. M., van Aken, H. M., Sintes, E. & Herndl, G. J. Latitudinal trends of Crenarchaeota and Bacteria in the meso- and bathypelagic water masses of the Eastern North Atlantic. Environ. Microbiol. 10, 110–124 (2008)
Lam, P. et al. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl Acad. Sci. USA 104, 7104–7109 (2007)
Rhein, M. et al. Labrador Sea Water: pathways, CFC inventory, and formation rates. J. Phys. Oceanogr. 32, 648–665 (2002)
Hollibaugh, J. T., Bano, N. & Ducklow, H. W. Widespread distribution in polar oceans of a 16S rRNA gene sequence with affinity to Nitrosospira-like ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 68, 1478–1484 (2002)
Smethie, W. M. & Fine, R. A. Rates of North Atlantic Deep Water formation calculated from chlorofluorocarbon inventories. Deep-Sea Res. I 48, 189–215 (2001)
van Aken, H. M. The hydrography of the mid-latitude northeast Atlantic Ocean: I: the deep water masses. Deep-Sea Res. I 47, 757–788 (2000)
Hallam, S. J. et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, 520–536 (2006)
Berg, I. A., Kockelkorn, D., Buckel, W. & Fuchs, G. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. Science 318, 1782–1786 (2007)
Martin-Cuadrado, A.-B. et al. Hindsight in the relative abundance, metabolic potential and genome dynamics of uncultivated marine archaea from comparative metagenomic analyses of bathypelagic plankton of different oceanic regions. ISME J. 2, 865–886 (2008)
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.
Author information
Authors and Affiliations
Corresponding author
Supplementary information
Supplementary Information
This file contains Supplementary Methods, a Supplementary Discussion, Supplementary Tables S1-S4, Supplementary Figures S1-S5 with legends and additional references. (PDF 1537 kb)
Rights and permissions
About this article
Cite this article
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). https://doi.org/10.1038/nature07535
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature07535
This article is cited by
-
Vertical segregation and phylogenetic characterization of archaea and archaeal ammonia monooxygenase gene in the water column of the western Arctic Ocean
Extremophiles (2023)
-
Marine ammonia-oxidising archaea and bacteria occupy distinct iron and copper niches
ISME Communications (2021)
-
Genome-resolved metagenomics analysis provides insights into the ecological role of Thaumarchaeota in the Amazon River and its plume
BMC Microbiology (2020)
-
Metagenome-assembled genomes reveal unique metabolic adaptations of a basal marine Thaumarchaeota lineage
The ISME Journal (2020)
-
Distinct distribution patterns of ammonia-oxidizing archaea and bacteria in sediment and water column of the Yellow River estuary
Scientific Reports (2018)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.