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A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O

When oxygen becomes limiting, denitrifying bacteria must prepare for anaerobic respiration by synthesizing the reductases NAR (NO(3)(−) → NO(2)(−)), NIR (NO(2)(−) → NO), NOR (2NO → N(2)O), and NOS (N(2)O → N(2)), either en bloc or sequentially, to avoid entrapment in anoxia without energy. Minimizin...

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Autores principales: Lycus, Pawel, Soriano-Laguna, Manuel Jesús, Kjos, Morten, Richardson, David John, Gates, Andrew James, Milligan, Daniel Aleksanteri, Frostegård, Åsa, Bergaust, Linda, Bakken, Lars Reier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6243289/
https://www.ncbi.nlm.nih.gov/pubmed/30385636
http://dx.doi.org/10.1073/pnas.1805000115
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author Lycus, Pawel
Soriano-Laguna, Manuel Jesús
Kjos, Morten
Richardson, David John
Gates, Andrew James
Milligan, Daniel Aleksanteri
Frostegård, Åsa
Bergaust, Linda
Bakken, Lars Reier
author_facet Lycus, Pawel
Soriano-Laguna, Manuel Jesús
Kjos, Morten
Richardson, David John
Gates, Andrew James
Milligan, Daniel Aleksanteri
Frostegård, Åsa
Bergaust, Linda
Bakken, Lars Reier
author_sort Lycus, Pawel
collection PubMed
description When oxygen becomes limiting, denitrifying bacteria must prepare for anaerobic respiration by synthesizing the reductases NAR (NO(3)(−) → NO(2)(−)), NIR (NO(2)(−) → NO), NOR (2NO → N(2)O), and NOS (N(2)O → N(2)), either en bloc or sequentially, to avoid entrapment in anoxia without energy. Minimizing the metabolic burden of this precaution is a plausible fitness trait, and we show that the model denitrifier Paracoccus denitrificans achieves this by synthesizing NOS in all cells, while only a minority synthesize NIR. Phenotypic diversification with regards to NIR is ascribed to stochastic initiation of gene transcription, which becomes autocatalytic via NO production. Observed gas kinetics suggest that such bet hedging is widespread among denitrifying bacteria. Moreover, in response to oxygenation, P. denitrificans preserves NIR in the poles of nongrowing persister cells, ready to switch to anaerobic respiration in response to sudden anoxia. Our findings add dimensions to the regulatory biology of denitrification and identify regulatory traits that decrease N(2)O emissions.
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spelling pubmed-62432892018-11-27 A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O Lycus, Pawel Soriano-Laguna, Manuel Jesús Kjos, Morten Richardson, David John Gates, Andrew James Milligan, Daniel Aleksanteri Frostegård, Åsa Bergaust, Linda Bakken, Lars Reier Proc Natl Acad Sci U S A Biological Sciences When oxygen becomes limiting, denitrifying bacteria must prepare for anaerobic respiration by synthesizing the reductases NAR (NO(3)(−) → NO(2)(−)), NIR (NO(2)(−) → NO), NOR (2NO → N(2)O), and NOS (N(2)O → N(2)), either en bloc or sequentially, to avoid entrapment in anoxia without energy. Minimizing the metabolic burden of this precaution is a plausible fitness trait, and we show that the model denitrifier Paracoccus denitrificans achieves this by synthesizing NOS in all cells, while only a minority synthesize NIR. Phenotypic diversification with regards to NIR is ascribed to stochastic initiation of gene transcription, which becomes autocatalytic via NO production. Observed gas kinetics suggest that such bet hedging is widespread among denitrifying bacteria. Moreover, in response to oxygenation, P. denitrificans preserves NIR in the poles of nongrowing persister cells, ready to switch to anaerobic respiration in response to sudden anoxia. Our findings add dimensions to the regulatory biology of denitrification and identify regulatory traits that decrease N(2)O emissions. National Academy of Sciences 2018-11-13 2018-11-01 /pmc/articles/PMC6243289/ /pubmed/30385636 http://dx.doi.org/10.1073/pnas.1805000115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Lycus, Pawel
Soriano-Laguna, Manuel Jesús
Kjos, Morten
Richardson, David John
Gates, Andrew James
Milligan, Daniel Aleksanteri
Frostegård, Åsa
Bergaust, Linda
Bakken, Lars Reier
A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O
title A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O
title_full A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O
title_fullStr A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O
title_full_unstemmed A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O
title_short A bet-hedging strategy for denitrifying bacteria curtails their release of N(2)O
title_sort bet-hedging strategy for denitrifying bacteria curtails their release of n(2)o
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6243289/
https://www.ncbi.nlm.nih.gov/pubmed/30385636
http://dx.doi.org/10.1073/pnas.1805000115
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