Cyanate as an energy source for nitrifiers.

Abstract

Ammonia- and nitrite-oxidizers are collectively responsible for the aerobic oxidation of ammonia via nitrite to nitrate and play essential roles for the global biogeochemical nitrogen cycle. The physiology of these nitrifying microbes has been intensively studied since the first experiments of Sergei Winogradsky more than a century ago. Urea and ammonia are the only recognized energy sources that promote the aerobic growth of ammonia-oxidizing bacteria and archaea. Here we report the aerobic growth of a pure culture of the ammonia-oxidizing thaumarchaeote Nitrososphaera gargensis1 on cyanate as the sole source of energy and reductant, the first organism known to do so. Cyanate, which is a potentially important source of reduced nitrogen in aquatic and terrestrial ecosystems2, is converted to ammonium and CO2 by this archaeon using a cyanase that is induced upon addition of this compound. Within the cyanase gene family, this cyanase is a member of a distinct clade that also contains cyanases of nitrite-oxidizing bacteria of the genus Nitrospira. We demonstrate by co-culture experiments that these nitrite-oxidizers supply ammonia-oxidizers lacking cyanase with ammonium from cyanate, which is fully nitrified by this consortium through reciprocal feeding. Screening of a comprehensive set of more than 3,000 publically available metagenomes from environmental samples revealed that cyanase-encoding genes clustering with the cyanases of these nitrifiers are widespread in the environment. Our results demonstrate an unexpected metabolic versatility of nitrifying microbes and suggest a previously unrecognized importance of cyanate for N-cycling in the environment.