Copper requirements of the ammonia-oxidizing archaeon Nitrosopumilus maritimus SCM1 and implications for nitrification in the marine environment

Shady A. Amin, James W. Moffett, Willm Martens-Habbena, Jeremy E. Jacquot, Yang Han, Allan Devol, Anitra E. Ingalls, David A. Stahl and E. Virginia Armbrust

Limnol. Oceanogr., 58(6), 2013, 2037-2045 | DOI: 10.4319/lo.2013.58.6.2037

ABSTRACT: Ammonia oxidizing archaea (AOA) have recently been recognized as the primary nitrifiers in the marine environment; they thus play an important role in the nitrogen cycle. Available genome sequences of AOA indicate that numerous Cu-dependent enzymes are essential for both ammonia oxidation and electron transfer, suggesting a particularly high requirement for copper. However, our knowledge of the copper requirements of AOA and their response to copper limitation in the ocean is nonexistent. Here, we examine the copper requirements of the chemolithoautotrophic AOA Candidatus Nitrosopumilus maritimus SCM1 using a combination of the metal chelators ethylenediaminetetraacetic acid and 1,4,8,11-tetraazacyclotetradecane-1,4,8,11-tetraacetic acid and show that ammonia oxidation is limited at free cupric ion concentrations < 10−12.7 mol L−1, which are higher than concentrations frequently reported for many coastal and oceanic regimes. Prolonged exposure of cells to copper starvation for up to 6 d had no effect on the recovery of ammonia oxidation by N. maritimus. In addition, we present evidence that N. maritimus does not produce a copper-binding ligand (chalkophore) under copper limitation and therefore probably relies mainly on acquisition of copper ions from surrounding media. Copper limitation may be an important constraint on archaeal ammonia oxidation throughout the marine environment.

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