Archaeal nitrification in the ocean

doi:10.1073/pnas.0600756103

Archaeal nitrification in the ocean

*Departments of Marine Biogeochemistry and Toxicology and of Biological Oceanography, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB, Den Burg, The Netherlands;
^‡Department of Microbiology, Radboud University Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands; and
^¶Centre for Estuarine and Marine Ecology, Netherlands Institute for Ecology (NIOO-KNAW), P.O. Box 140, 4400 AC, Yerseke, The Netherlands

Edited by Carl R. Woese, University of Illinois at Urbana–Champaign, Urbana, IL, and approved June 6, 2006 (received for review January 30, 2006)

Abstract

Marine Crenarchaeota are the most abundant single group of prokaryotes in the ocean, but their physiology and role in marine biogeochemical cycles are unknown. Recently, a member of this clade was isolated from a sea aquarium and shown to be capable of nitrification, tentatively suggesting that Crenarchaeota may play a role in the oceanic nitrogen cycle. We enriched a crenarchaeote from North Sea water and showed that its abundance, and not that of bacteria, correlates with ammonium oxidation to nitrite. A time series study in the North Sea revealed that the abundance of the gene encoding for the archaeal ammonia monooxygenase alfa subunit (amoA) is correlated with a decline in ammonium concentrations and with the abundance of Crenarchaeota. Remarkably, the archaeal amoA abundance was 1–2 orders of magnitude higher than those of bacterial nitrifiers, which are commonly thought to mediate the oxidation of ammonium to nitrite in marine environments. Analysis of Atlantic waters of the upper 1,000 m, where most of the ammonium regeneration and oxidation takes place, showed that crenarchaeotal amoA copy numbers are also 1–3 orders of magnitude higher than those of bacterial amoA. Our data thus suggest a major role for Archaea in oceanic nitrification.

Footnotes

^¶To whom correspondence should be addressed. E-mail: damste{at}nioz.nl
↵ ^†Present address: Woods Hole Oceanographic Institution, Department of Chemistry and Geochemistry, 360 Woods Hole Road, Woods Hole, MA 02543.
↵ ^§Present address: Departamento Ecoloxía e Bioloxía Animal, Universidade de Vigo, Campus Lagoas–Marcosende, 36200 Vigo, Spain.
Author contributions: C.W., M.J.L.C., S.S., and J.S.S.D. designed research; C.W., B.A., L.H., and P.T. performed research; M.J.L.C., J.v.B., E.T., and G.J.H. contributed new reagents/analytic tools; C.W., M.J.L.C., J.v.B., M.S., G.J.H., J.J.M., S.S., and J.S.S.D. analyzed data; and M.J.L.C., M.S., J.J.M., S.S., and J.S.S.D. wrote the paper.
Conflict of interest statement: No conflicts declared.
This paper was submitted directly (Track II) to the PNAS office.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. DQ659389–DQ659410 (archaeal 16S rDNA) and DQ784527–DQ784538 (amoA)].
Abbreviations:

Abbreviations

AOB,

ammonia-oxidizing bacteria;

CARD-FISH,

catalyzed reporter deposition–FISH;

DGGE,

denaturing gradient gel electrophoresis;

QPCR,

quantitative PCR.
Freely available online through the PNAS open access option.