Anaerobic ammonium oxidation by anammox bacteria in the Black Sea

Kuypers, Marcel M. M.
Sliekers, Olav A.
Lavik, Gaute
Schmid, Markus
Jørgensen, Bo Barker
Kuenen, Gijs J.
Damsté, Jaap S. Sinninghe
Strous, Marc
Jetten, Mike S. M.

* Max Planck Institute for Marine Microbiology (MPI), Department of Biogeochemistry, Celsiusstrasse 1, 28359 Bremen, Germany
† Department of Microbiology, Delft University of Technology, Julianalaan 67, 2628 BC Delft, The Netherlands
‡ Royal Netherlands Institute for Sea Research (NIOZ), Department of Marine Biogeochemistry and Toxicology, PO Box 59, 1790 AB Den Burg, The Netherlands
§ Department of Microbiology, University of Nijmegen, Toernooiveld 1, 6526 ED Nijmegen, The Netherlands

Received 8 November 2002; accepted 3 February 2003; doi:10.1038/nature01472.

Correspondence and requests for materials should be addressed to M.M.M.K.

Nature 422(6932):p 608-611, April 10, 2003.

The availability of fixed inorganic nitrogen (nitrate, nitrite and ammonium) limits primary productivity in many oceanic regions. The conversion of nitrate to N₂ by heterotrophic bacteria (denitrification) is believed to be the only important sink for fixed inorganic nitrogen in the ocean. Here we provide evidence for bacteria that anaerobically oxidize ammonium with nitrite to N₂ in the world's largest anoxic basin, the Black Sea. Phylogenetic analysis of 16S ribosomal RNA gene sequences shows that these bacteria are related to members of the order Planctomycetales performing the anammox (anaerobic ammonium oxidation) process in ammonium-removing bioreactors. Nutrient profiles, fluorescently labelled RNA probes, ¹⁵N tracer experiments and the distribution of specific ‘ladderane’ membrane lipidsindicate that ammonium diffusing upwards from the anoxic deep water is consumed by anammox bacteria below the oxic zone. This is the first time that anammox bacteria have been identified and directly linked to the removal of fixed inorganic nitrogen in the environment. The widespread occurrence of ammonium consumption in suboxic marine settingsindicates that anammox might be important in the oceanic nitrogen cycle.