Role for urea in nitrification by polar marine Archaea

Laura Alonso-Sáez; Alison S. Waller; Daniel R. Mende; Kevin Bakker; Hanna Farnelid; Patricia L. Yager; Connie Lovejoy; Jean-Éric Tremblay; Marianne Potvin; Friederike Heinrich; Marta Estrada; Lasse Riemann; Peer Bork; Carlos Pedrós-Alió; Stefan Bertilsson

doi:10.1073/pnas.1201914109

Role for urea in nitrification by polar marine Archaea

Laura Alonso-Sáez, Alison S. Waller, Daniel R. Mende, Kevin Bakker, Hanna Farnelid, Patricia L. Yager, Connie Lovejoy, Jean-Éric Tremblay, Marianne Potvin, Friederike Heinrich, Marta Estrada, Lasse Riemann, Peer Bork, Carlos Pedrós-Alió, Stefan Bertilsson

Marine Biology

158 Citations (Scopus)

Abstract

Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.

Original language	English
Journal	Proceedings of the National Academy of Sciences USA (PNAS)
Volume	109
Issue number	44
Pages (from-to)	17989-17994
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1201914109
Publication status	Published - 30 Oct 2012

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Alonso-Sáez, L., Waller, A. S., Mende, D. R., Bakker, K., Farnelid, H., Yager, P. L., Lovejoy, C., Tremblay, J-É., Potvin, M., Heinrich, F., Estrada, M., Riemann, L., Bork, P., Pedrós-Alió, C., & Bertilsson, S. (2012). Role for urea in nitrification by polar marine Archaea. Proceedings of the National Academy of Sciences USA (PNAS), 109(44), 17989-17994. https://doi.org/10.1073/pnas.1201914109

Alonso-Sáez, L, Waller, AS, Mende, DR, Bakker, K, Farnelid, H, Yager, PL, Lovejoy, C, Tremblay, J-É, Potvin, M, Heinrich, F, Estrada, M, Riemann, L, Bork, P, Pedrós-Alió, C & Bertilsson, S 2012, 'Role for urea in nitrification by polar marine Archaea', Proceedings of the National Academy of Sciences USA (PNAS), vol. 109, no. 44, pp. 17989-17994. https://doi.org/10.1073/pnas.1201914109

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title = "Role for urea in nitrification by polar marine Archaea",

abstract = "Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.",

author = "Laura Alonso-S{\'a}ez and Waller, {Alison S.} and Mende, {Daniel R.} and Kevin Bakker and Hanna Farnelid and Yager, {Patricia L.} and Connie Lovejoy and Jean-{\'E}ric Tremblay and Marianne Potvin and Friederike Heinrich and Marta Estrada and Lasse Riemann and Peer Bork and Carlos Pedr{\'o}s-Ali{\'o} and Stefan Bertilsson",

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T1 - Role for urea in nitrification by polar marine Archaea

AU - Alonso-Sáez, Laura

AU - Waller, Alison S.

AU - Mende, Daniel R.

AU - Bakker, Kevin

AU - Farnelid, Hanna

AU - Yager, Patricia L.

AU - Lovejoy, Connie

AU - Tremblay, Jean-Éric

AU - Potvin, Marianne

AU - Heinrich, Friederike

AU - Estrada, Marta

AU - Riemann, Lasse

AU - Bork, Peer

AU - Pedrós-Alió, Carlos

AU - Bertilsson, Stefan

PY - 2012/10/30

Y1 - 2012/10/30

N2 - Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.

AB - Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.

U2 - 10.1073/pnas.1201914109

DO - 10.1073/pnas.1201914109

M3 - Journal article

C2 - 23027926

SN - 0027-8424

VL - 109

SP - 17989

EP - 17994

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 44

ER -

Role for urea in nitrification by polar marine Archaea

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