Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth

ABSTRACT Ammonia-oxidizing microorganisms perform the first step of nitrification, the oxidation of ammonia to nitrite. The bacterium Nitrosomonas europaea is the best-characterized ammonia oxidizer to date. Exposure to hypoxic conditions has a profound effect on the physiology of N. europaea, e.g.,...

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Autores principales:	Christopher J. Sedlacek, Andrew T. Giguere, Michael D. Dobie, Brett L. Mellbye, Rebecca V. Ferrell, Dagmar Woebken, Luis A. Sayavedra-Soto, Peter J. Bottomley, Holger Daims, Michael Wagner, Petra Pjevac
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	ammonia and oxygen limitation ammonia-oxidizing bacteria chemostat nitrification Nitrosomonas europaea transcriptome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/725ca93cf8d94a10af17c9d19b0576cd
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spelling	oai:doaj.org-article:725ca93cf8d94a10af17c9d19b0576cd2021-12-02T18:44:38ZTranscriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth10.1128/mSystems.00562-192379-5077https://doaj.org/article/725ca93cf8d94a10af17c9d19b0576cd2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00562-19https://doaj.org/toc/2379-5077ABSTRACT Ammonia-oxidizing microorganisms perform the first step of nitrification, the oxidation of ammonia to nitrite. The bacterium Nitrosomonas europaea is the best-characterized ammonia oxidizer to date. Exposure to hypoxic conditions has a profound effect on the physiology of N. europaea, e.g., by inducing nitrifier denitrification, resulting in increased nitric and nitrous oxide production. This metabolic shift is of major significance in agricultural soils, as it contributes to fertilizer loss and global climate change. Previous studies investigating the effect of oxygen limitation on N. europaea have focused on the transcriptional regulation of genes involved in nitrification and nitrifier denitrification. Here, we combine steady-state cultivation with whole-genome transcriptomics to investigate the overall effect of oxygen limitation on N. europaea. Under oxygen-limited conditions, growth yield was reduced and ammonia-to-nitrite conversion was not stoichiometric, suggesting the production of nitrogenous gases. However, the transcription of the principal nitric oxide reductase (cNOR) did not change significantly during oxygen-limited growth, while the transcription of the nitrite reductase-encoding gene (nirK) was significantly lower. In contrast, both heme-copper-containing cytochrome c oxidases encoded by N. europaea were upregulated during oxygen-limited growth. Particularly striking was the significant increase in transcription of the B-type heme-copper oxidase, proposed to function as a nitric oxide reductase (sNOR) in ammonia-oxidizing bacteria. In the context of previous physiological studies, as well as the evolutionary placement of N. europaea’s sNOR with regard to other heme-copper oxidases, these results suggest sNOR may function as a high-affinity terminal oxidase in N. europaea and other ammonia-oxidizing bacteria. IMPORTANCE Nitrification is a ubiquitous microbially mediated process in the environment and an essential process in engineered systems such as wastewater and drinking water treatment plants. However, nitrification also contributes to fertilizer loss from agricultural environments, increasing the eutrophication of downstream aquatic ecosystems, and produces the greenhouse gas nitrous oxide. As ammonia-oxidizing bacteria are the most dominant ammonia-oxidizing microbes in fertilized agricultural soils, understanding their responses to a variety of environmental conditions is essential for curbing the negative environmental effects of nitrification. Notably, oxygen limitation has been reported to significantly increase nitric oxide and nitrous oxide production during nitrification. Here, we investigate the physiology of the best-characterized ammonia-oxidizing bacterium, Nitrosomonas europaea, growing under oxygen-limited conditions.Christopher J. SedlacekAndrew T. GiguereMichael D. DobieBrett L. MellbyeRebecca V. FerrellDagmar WoebkenLuis A. Sayavedra-SotoPeter J. BottomleyHolger DaimsMichael WagnerPetra PjevacAmerican Society for Microbiologyarticleammonia and oxygen limitationammonia-oxidizing bacteriachemostatnitrificationNitrosomonas europaeatranscriptomeMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	ammonia and oxygen limitation ammonia-oxidizing bacteria chemostat nitrification Nitrosomonas europaea transcriptome Microbiology QR1-502
spellingShingle	ammonia and oxygen limitation ammonia-oxidizing bacteria chemostat nitrification Nitrosomonas europaea transcriptome Microbiology QR1-502 Christopher J. Sedlacek Andrew T. Giguere Michael D. Dobie Brett L. Mellbye Rebecca V. Ferrell Dagmar Woebken Luis A. Sayavedra-Soto Peter J. Bottomley Holger Daims Michael Wagner Petra Pjevac Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth
description	ABSTRACT Ammonia-oxidizing microorganisms perform the first step of nitrification, the oxidation of ammonia to nitrite. The bacterium Nitrosomonas europaea is the best-characterized ammonia oxidizer to date. Exposure to hypoxic conditions has a profound effect on the physiology of N. europaea, e.g., by inducing nitrifier denitrification, resulting in increased nitric and nitrous oxide production. This metabolic shift is of major significance in agricultural soils, as it contributes to fertilizer loss and global climate change. Previous studies investigating the effect of oxygen limitation on N. europaea have focused on the transcriptional regulation of genes involved in nitrification and nitrifier denitrification. Here, we combine steady-state cultivation with whole-genome transcriptomics to investigate the overall effect of oxygen limitation on N. europaea. Under oxygen-limited conditions, growth yield was reduced and ammonia-to-nitrite conversion was not stoichiometric, suggesting the production of nitrogenous gases. However, the transcription of the principal nitric oxide reductase (cNOR) did not change significantly during oxygen-limited growth, while the transcription of the nitrite reductase-encoding gene (nirK) was significantly lower. In contrast, both heme-copper-containing cytochrome c oxidases encoded by N. europaea were upregulated during oxygen-limited growth. Particularly striking was the significant increase in transcription of the B-type heme-copper oxidase, proposed to function as a nitric oxide reductase (sNOR) in ammonia-oxidizing bacteria. In the context of previous physiological studies, as well as the evolutionary placement of N. europaea’s sNOR with regard to other heme-copper oxidases, these results suggest sNOR may function as a high-affinity terminal oxidase in N. europaea and other ammonia-oxidizing bacteria. IMPORTANCE Nitrification is a ubiquitous microbially mediated process in the environment and an essential process in engineered systems such as wastewater and drinking water treatment plants. However, nitrification also contributes to fertilizer loss from agricultural environments, increasing the eutrophication of downstream aquatic ecosystems, and produces the greenhouse gas nitrous oxide. As ammonia-oxidizing bacteria are the most dominant ammonia-oxidizing microbes in fertilized agricultural soils, understanding their responses to a variety of environmental conditions is essential for curbing the negative environmental effects of nitrification. Notably, oxygen limitation has been reported to significantly increase nitric oxide and nitrous oxide production during nitrification. Here, we investigate the physiology of the best-characterized ammonia-oxidizing bacterium, Nitrosomonas europaea, growing under oxygen-limited conditions.
format	article
author	Christopher J. Sedlacek Andrew T. Giguere Michael D. Dobie Brett L. Mellbye Rebecca V. Ferrell Dagmar Woebken Luis A. Sayavedra-Soto Peter J. Bottomley Holger Daims Michael Wagner Petra Pjevac
author_facet	Christopher J. Sedlacek Andrew T. Giguere Michael D. Dobie Brett L. Mellbye Rebecca V. Ferrell Dagmar Woebken Luis A. Sayavedra-Soto Peter J. Bottomley Holger Daims Michael Wagner Petra Pjevac
author_sort	Christopher J. Sedlacek
title	Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth
title_short	Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth
title_full	Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth
title_fullStr	Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth
title_full_unstemmed	Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth
title_sort	transcriptomic response of <named-content content-type="genus-species">nitrosomonas europaea</named-content> transitioned from ammonia- to oxygen-limited steady-state growth
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/725ca93cf8d94a10af17c9d19b0576cd
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Transcriptomic Response of <named-content content-type="genus-species">Nitrosomonas europaea</named-content> Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth

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