title: Cyanate as an energy source for nitrifiers.
abstract: 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 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, 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.
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Marton
authors.initials: M
authors.lastname: Palatinszky
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Craig
authors.initials: C
authors.lastname: Herbold
authors.affiliation: Department of Proteomics, Helmholtz Centre for Environmental Research - UFZ, Permoserstr. 15, 04318 Leipzig, Germany.
authors.forename: Nico
authors.initials: N
authors.lastname: Jehmlich
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Mario
authors.initials: M
authors.lastname: Pogoda
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Ping
authors.initials: P
authors.lastname: Han
authors.affiliation: 1] Department of Proteomics, Helmholtz Centre for Environmental Research - UFZ, Permoserstr. 15, 04318 Leipzig, Germany [2] Department of Metabolomics, Helmholtz Centre for Environmental Research - UFZ, Permoserstr. 15, 04318 Leipzig, Germany [3] Department of Chemistry and Bioscience, The Faculty of Engineering and Science, Aalborg University, Fredrik Bajers Vej 7, 9220 Aalborg, Denmark.
authors.forename: Martin
authors.initials: M
authors.lastname: von Bergen
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Ilias
authors.initials: I
authors.lastname: Lagkouvardos
authors.affiliation: Department of Chemistry and Bioscience, The Faculty of Engineering and Science, Aalborg University, Fredrik Bajers Vej 7, 9220 Aalborg, Denmark.
authors.forename: Søren M
authors.initials: SM
authors.lastname: Karst
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Alexander
authors.initials: A
authors.lastname: Galushko
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Hanna
authors.initials: H
authors.lastname: Koch
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: David
authors.initials: D
authors.lastname: Berry
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Holger
authors.initials: H
authors.lastname: Daims
authors.affiliation: Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
authors.forename: Michael
authors.initials: M
authors.lastname: Wagner
mesh_terms: D000332:Aerobiosis; D000641:Ammonia / Q000378:metabolism; D064751:Ammonium Compounds / Q000378:metabolism; D001105:Archaea / Q000201:enzymology / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D002245:Carbon Dioxide / Q000378:metabolism; D019759:Carbon-Nitrogen Lyases / Q000235:genetics / Q000378:metabolism; D003485:Cyanates / Q000378:metabolism*; D004783:Environmental Microbiology; D054892:Metagenome / Q000235:genetics; D009566:Nitrates / Q000378:metabolism; D058465:Nitrification; D009573:Nitrites / Q000378:metabolism; D009584:Nitrogen / Q000378:metabolism; D058458:Nitrogen Cycle; D010084:Oxidation-Reduction
chemical_list: D064751:Ammonium Compounds; D003485:Cyanates; D009566:Nitrates; D009573:Nitrites; D002245:Carbon Dioxide; D000641:Ammonia; C019953:cyanate hydrolase; D019759:Carbon-Nitrogen Lyases; D009584:Nitrogen