Transcriptomic Response of Nitrosomonas europaea Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth

Sedlacek, Christopher J.; Giguere, Andrew T.; Dobie, Michael D.; Mellbye, Brett L.; Ferrell, Rebecca V.; Woebken, Dagmar; Sayavedra-Soto, Luis A.; Bottomley, Peter J.; Daims, Holger; Wagner, Michael; Pjevac, Petra

doi:10.1128/msystems.00562-19

Title: Transcriptomic Response of Nitrosomonas europaea Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth

Journal Article · 13 January 2020 · mSystems

DOI: https://doi.org/10.1128/msystems.00562-19 · OSTI ID:1626184

Sedlacek, Christopher J. ^[1]; Giguere, Andrew T. ^[2]; Dobie, Michael D. ^[3]; Mellbye, Brett L. ^[3]; Ferrell, Rebecca V. ^[4]; Woebken, Dagmar ^[5]; Sayavedra-Soto, Luis A. ^[6]; Bottomley, Peter J. ^[7]; Daims, Holger ^[8]; Wagner, Michael ^[9]; Pjevac, Petra ^[10]

Univ. of Vienna (Austria). Centre for Microbiology and Environmental Systems Science. Division of Microbial Ecology; Univ. of Vienna (Austria). The Comammox Research Platform; DOE/OSTI
Univ. of Vienna (Austria). Centre for Microbiology and Environmental Systems Science. Division of Microbial Ecology; Oregon State Univ., Corvallis, OR (United States). Dept. of Crop and Soil Science; Aalborg Univ. (Denmark). Dept. of Chemistry and Bioscience. Center for Microbial Communities
Oregon State Univ., Corvallis, OR (United States). Dept. of Microbiology
Metropolitan State Univ. of Denver, CO (United States). Dept. of Biology
Univ. of Vienna (Austria). Centre for Microbiology and Environmental Systems Science. Division of Microbial Ecology
Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology
Oregon State Univ., Corvallis, OR (United States). Dept. of Crop and Soil Science; Oregon State Univ., Corvallis, OR (United States). Dept. of Microbiology
Univ. of Vienna (Austria). Centre for Microbiology and Environmental Systems Science. Division of Microbial Ecology; Univ. of Vienna (Austria). The Comammox Research Platform
Univ. of Vienna (Austria). Centre for Microbiology and Environmental Systems Science. Division of Microbial Ecology; Univ. of Vienna (Austria). The Comammox Research Platform; Aalborg Univ. (Denmark). Dept. of Chemistry and Bioscience. Center for Microbial Communities
Univ. of Vienna (Austria). Centre for Microbiology and Environmental Systems Science. Division of Microbial Ecology; Univ. of Vienna (Austria). Joint Microbiome Facility of the Medical Univ. of Vienna

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.

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Research Organization:: Oregon State Univ., Corvallis, OR (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626184

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 1 Vol. 5; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cytochromes P460 and c ′-beta; A new family of high-spin cytochromes c Elmore, Bradley O.; Bergmann, David J.; Klotz, Martin G. FEBS Letters, Vol. 581, Issue 5 https://doi.org/10.1016/j.febslet.2007.01.068	journal	February 2007
Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme?copper oxidase type Zumft, W. Journal of Inorganic Biochemistry, Vol. 99, Issue 1 https://doi.org/10.1016/j.jinorgbio.2004.09.024	journal	January 2005
Alternative Bioenergy: Updates to and Challenges in Nitrification Metalloenzymology Lancaster, Kyle M.; Caranto, Jonathan D.; Majer, Sean H. Joule, Vol. 2, Issue 3 https://doi.org/10.1016/j.joule.2018.01.018	journal	March 2018
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Additional file 3 of Revealing taxon-specific heavy metal-resistance mechanisms in denitrifying phosphorus removal sludge using genome-centric metaproteomics Lin, Yuan; Wang, Liye; Xu, Ke figshare https://doi.org/10.6084/m9.figshare.14266765.v1	dataset	January 2021
Additional file 4 of Revealing taxon-specific heavy metal-resistance mechanisms in denitrifying phosphorus removal sludge using genome-centric metaproteomics Lin, Yuan; Wang, Liye; Xu, Ke figshare https://doi.org/10.6084/m9.figshare.14266768	dataset	January 2021
Additional file 5 of Revealing taxon-specific heavy metal-resistance mechanisms in denitrifying phosphorus removal sludge using genome-centric metaproteomics Lin, Yuan; Wang, Liye; Xu, Ke figshare https://doi.org/10.6084/m9.figshare.14266771.v1	dataset	January 2021

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