Journal Article

Cyanate as an energy source for nitrifiers

Daims, Holger, Lagkouvardos, Ilias, Galushko, Alexander, Han, Ping, Karst, Søren M., Koch, Hanna, Pogoda, Mario, von Bergen, Martin, Berry, David, Palatinszky, Marton, Wagner, Michael, Herbold, Craig, Jehmlich, Nico

2015

Overview

The ammonia-oxidizing archaeon Nitrososphaera gargensis can utilize cyanate as the only source of energy for growth due to the presence of a cyanase enzyme, and cyanase-encoding nitrite-oxidizing bacteria can work together with cyanase-negative ammonia oxidizers to collectively grow on cyanate via reciprocal feeding; cyanases are widespread in the environment according to metagenomic data sets, pointing to the potential importance of cyanate in the nitrogen cycle. Cyanate an unexpected energy source Nitrification is a central process in the global nitrogen cycle and plays a major role in fertilizer loss in industrial agriculture. Here Michael Wagner and colleagues report that the ammonia-oxidizing archaeon Nitrosphaera gargensis can grow on cyanate as its sole energy source — possibly the only known organism capable of doing so. The archaeon converts cyanate to ammonium and carbon dioxide using a cyanase enzyme. Further investigation of metagenomes shows that cyanases are widespread in the environment. This work highlights the potential importance of cyanate in the nitrogen cycle as a source of reduced nitrogen in the environment. Ammonia- and nitrite-oxidizing microorganisms are collectively responsible for the aerobic oxidation of ammonia via nitrite to nitrate and have essential roles in the global biogeochemical nitrogen cycle. The physiology of nitrifiers has been intensively studied, and 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 gargensis 1 using cyanate as the sole source of energy and reductant; to our knowledge, the first organism known to do so. Cyanate, a potentially important source of reduced nitrogen in aquatic and terrestrial ecosystems 2 , is converted to ammonium and carbon dioxide in Nitrososphaera gargensis by a cyanase enzyme that is induced upon addition of this compound. Within the cyanase gene family, this cyanase is a member of a distinct clade also containing cyanases of nitrite-oxidizing bacteria of the genus Nitrospira. We demonstrate by co-culture experiments that these nitrite oxidizers supply cyanase-lacking ammonia oxidizers with ammonium from cyanate, which is fully nitrified by this microbial consortium through reciprocal feeding. By screening a comprehensive set of more than 3,000 publically available metagenomes from environmental samples, we reveal 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 microorganisms, and suggest a previously unrecognized importance of cyanate in cycling of nitrogen compounds in the environment.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14/19 / 38/32 / 38/77 / 45 / 631/326/171 / 631/326/2565 / 82 / 82/58 / Aerobiosis / Ammonia / Ammonia - metabolism / Ammonium / Ammonium Compounds - metabolism / Archaea - enzymology / Archaea - genetics / Archaea - growth & development / Archaea - metabolism / Biogeochemical cycles / Carbon dioxide / Carbon Dioxide - metabolism / Carbon-Nitrogen Lyases - genetics / Carbon-Nitrogen Lyases - metabolism / Chemical properties / Cyanates / Cyanates - metabolism / Decomposition / Energy sources / Environmental aspects / Environmental Microbiology / Enzymes / Genes / Genomes / Genomics / Humanities and Social Sciences / Ions / letter / Metabolism / Metagenome - genetics / Microorganisms / multidisciplinary / Nitrates - metabolism / Nitrification / Nitrites - metabolism / Nitrogen - metabolism / Nitrogen Cycle / Oxidation / Oxidation-Reduction / Proteins / Science / Terrestrial ecosystems / Urea