Cyanate as energy source for nitrifiers

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

Publikation: Bidrag til tidsskriftLetterForskningpeer review

84 Citationer (Scopus)

Resumé

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 gargensis1 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 ecosystems2, 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.
OriginalsprogEngelsk
TidsskriftNature
Vol/bind524
Sider (fra-til)105-108
Antal sider4
ISSN0028-0836
DOI
StatusUdgivet - 6 aug. 2015

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ammonia
nitrite
ammonium
microorganism
bacterium
nitrogen cycle
gene
nitrogen compound
urea
physiology
energy source
cyanate
carbon dioxide
enzyme
nitrate
oxidation
nitrogen
energy
experiment

Citer dette

Palatinszky, M., Herbold, C., Jehmlich, N., Pogoda, M., Han, P., von Bergen, M., ... Wagner, M. (2015). Cyanate as energy source for nitrifiers. Nature, 524, 105-108. https://doi.org/10.1038/nature14856
Palatinszky, Marton ; Herbold, Craig ; Jehmlich, Nico ; Pogoda, Mario ; Han, Ping ; von Bergen, Martin ; Lagkouvardos, Ilias ; Karst, Søren Michael ; Galushko, Alexander ; Koch, Hanna ; Berry, David ; Daims, Holger ; Wagner, Michael. / Cyanate as energy source for nitrifiers. I: Nature. 2015 ; Bind 524. s. 105-108.
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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 gargensis1 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 ecosystems2, 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.",
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Palatinszky, M, Herbold, C, Jehmlich, N, Pogoda, M, Han, P, von Bergen, M, Lagkouvardos, I, Karst, SM, Galushko, A, Koch, H, Berry, D, Daims, H & Wagner, M 2015, 'Cyanate as energy source for nitrifiers', Nature, bind 524, s. 105-108. https://doi.org/10.1038/nature14856

Cyanate as energy source for nitrifiers. / Palatinszky, Marton; Herbold, Craig; Jehmlich, Nico; Pogoda, Mario; Han, Ping; von Bergen, Martin; Lagkouvardos, Ilias; Karst, Søren Michael; Galushko, Alexander; Koch, Hanna; Berry, David; Daims, Holger; Wagner, Michael.

I: Nature, Bind 524, 06.08.2015, s. 105-108.

Publikation: Bidrag til tidsskriftLetterForskningpeer review

TY - JOUR

T1 - Cyanate as energy source for nitrifiers

AU - Palatinszky, Marton

AU - Herbold, Craig

AU - Jehmlich, Nico

AU - Pogoda, Mario

AU - Han, Ping

AU - von Bergen, Martin

AU - Lagkouvardos, Ilias

AU - Karst, Søren Michael

AU - Galushko, Alexander

AU - Koch, Hanna

AU - Berry, David

AU - Daims, Holger

AU - Wagner, Michael

PY - 2015/8/6

Y1 - 2015/8/6

N2 - 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 gargensis1 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 ecosystems2, 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.

AB - 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 gargensis1 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 ecosystems2, 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.

KW - nitrifier

KW - cyanate

KW - proteomics

KW - microbial ecology

KW - metagenomics

U2 - 10.1038/nature14856

DO - 10.1038/nature14856

M3 - Letter

VL - 524

SP - 105

EP - 108

JO - Nature

JF - Nature

SN - 0028-0836

ER -

Palatinszky M, Herbold C, Jehmlich N, Pogoda M, Han P, von Bergen M et al. Cyanate as energy source for nitrifiers. Nature. 2015 aug 6;524:105-108. https://doi.org/10.1038/nature14856