Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Man-Young Jung
  • Christopher J Sedlacek
  • K Dimitri Kits
  • Anna J Mueller
  • Sung-Keun Rhee
  • Linda Hink
  • Graeme W Nicol
  • Barbara Bayer
  • Laura Lehtovirta-Morley
  • Chloe Wright
  • Jose R de la Torre
  • Craig W Herbold
  • Petra Pjevac
  • Holger Daims
  • Michael Wagner

Research Organisations

External Research Organisations

  • University of Vienna
  • Chungbuk National University
  • University of East Anglia
  • San Francisco State University
  • École Centrale Lyon
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Details

Original languageEnglish
Pages (from-to)272-283
Number of pages12
JournalThe ISME journal
Volume16
Issue number1
Early online date27 Jul 2021
Publication statusPublished - Jan 2022

Abstract

Nitrification, the oxidation of ammonia to nitrate, is an essential process in the biogeochemical nitrogen cycle. The first step of nitrification, ammonia oxidation, is performed by three, often co-occurring guilds of chemolithoautotrophs: ammonia-oxidizing bacteria (AOB), archaea (AOA), and complete ammonia oxidizers (comammox). Substrate kinetics are considered to be a major niche-differentiating factor between these guilds, but few AOA strains have been kinetically characterized. Here, the ammonia oxidation kinetic properties of 12 AOA representing all major cultivated phylogenetic lineages were determined using microrespirometry. Members of the genus Nitrosocosmicus have the lowest affinity for both ammonia and total ammonium of any characterized AOA, and these values are similar to previously determined ammonia and total ammonium affinities of AOB. This contrasts previous assumptions that all AOA possess much higher substrate affinities than their comammox or AOB counterparts. The substrate affinity of ammonia oxidizers correlated with their cell surface area to volume ratios. In addition, kinetic measurements across a range of pH values supports the hypothesis that-like for AOB-ammonia and not ammonium is the substrate for the ammonia monooxygenase enzyme of AOA and comammox. Together, these data will facilitate predictions and interpretation of ammonia oxidizer community structures and provide a robust basis for establishing testable hypotheses on competition between AOB, AOA, and comammox.

ASJC Scopus subject areas

Cite this

Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities. / Jung, Man-Young; Sedlacek, Christopher J; Kits, K Dimitri et al.
In: The ISME journal, Vol. 16, No. 1, 01.2022, p. 272-283.

Research output: Contribution to journalArticleResearchpeer review

Jung, M-Y, Sedlacek, CJ, Kits, KD, Mueller, AJ, Rhee, S-K, Hink, L, Nicol, GW, Bayer, B, Lehtovirta-Morley, L, Wright, C, de la Torre, JR, Herbold, CW, Pjevac, P, Daims, H & Wagner, M 2022, 'Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities', The ISME journal, vol. 16, no. 1, pp. 272-283. https://doi.org/10.1038/s41396-021-01064-z
Jung, M.-Y., Sedlacek, C. J., Kits, K. D., Mueller, A. J., Rhee, S.-K., Hink, L., Nicol, G. W., Bayer, B., Lehtovirta-Morley, L., Wright, C., de la Torre, J. R., Herbold, C. W., Pjevac, P., Daims, H., & Wagner, M. (2022). Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities. The ISME journal, 16(1), 272-283. https://doi.org/10.1038/s41396-021-01064-z
Jung MY, Sedlacek CJ, Kits KD, Mueller AJ, Rhee SK, Hink L et al. Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities. The ISME journal. 2022 Jan;16(1):272-283. Epub 2021 Jul 27. doi: 10.1038/s41396-021-01064-z
Jung, Man-Young ; Sedlacek, Christopher J ; Kits, K Dimitri et al. / Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities. In: The ISME journal. 2022 ; Vol. 16, No. 1. pp. 272-283.
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abstract = "Nitrification, the oxidation of ammonia to nitrate, is an essential process in the biogeochemical nitrogen cycle. The first step of nitrification, ammonia oxidation, is performed by three, often co-occurring guilds of chemolithoautotrophs: ammonia-oxidizing bacteria (AOB), archaea (AOA), and complete ammonia oxidizers (comammox). Substrate kinetics are considered to be a major niche-differentiating factor between these guilds, but few AOA strains have been kinetically characterized. Here, the ammonia oxidation kinetic properties of 12 AOA representing all major cultivated phylogenetic lineages were determined using microrespirometry. Members of the genus Nitrosocosmicus have the lowest affinity for both ammonia and total ammonium of any characterized AOA, and these values are similar to previously determined ammonia and total ammonium affinities of AOB. This contrasts previous assumptions that all AOA possess much higher substrate affinities than their comammox or AOB counterparts. The substrate affinity of ammonia oxidizers correlated with their cell surface area to volume ratios. In addition, kinetic measurements across a range of pH values supports the hypothesis that-like for AOB-ammonia and not ammonium is the substrate for the ammonia monooxygenase enzyme of AOA and comammox. Together, these data will facilitate predictions and interpretation of ammonia oxidizer community structures and provide a robust basis for establishing testable hypotheses on competition between AOB, AOA, and comammox.",
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AU - Jung, Man-Young

AU - Sedlacek, Christopher J

AU - Kits, K Dimitri

AU - Mueller, Anna J

AU - Rhee, Sung-Keun

AU - Hink, Linda

AU - Nicol, Graeme W

AU - Bayer, Barbara

AU - Lehtovirta-Morley, Laura

AU - Wright, Chloe

AU - de la Torre, Jose R

AU - Herbold, Craig W

AU - Pjevac, Petra

AU - Daims, Holger

AU - Wagner, Michael

N1 - Funding Information: We would like to thank Márton Palatinszky, Ping Han, Michael Lukumbuzya, and Dimitra Sakoula for their assistance with microscopy and culture maintenance. CJS and DK were supported by the Wittgenstein award of the Austrian Science Fund FWF (Z383-B) to MW. PP and CJS were supported by the Austrian Science Fund FWF through the Young Investigators Research Grant program (ZK74). M-YJ was supported by the Research Institute for Basic Sciences (RIBS) of Jeju National University (2019R1A6A10072987) and the National research Facilities and Equipment Center of Korea Basic Science Institute (2020R1A6C101A188) through the National Research Foundation of Korea (NRF) grant funded by the Ministry of Education and MSIT (NRF-2021R1C1C1008303) by the Korea government. S-KR was supported by NRF grant funded by the Ministry of Environment (MOE) of the Republic of Korea (2021R1A2C3004015). CW was supported by a University of East Anglia-funded PhD studentship. LLM was supported by a Royal Society Dorothy Hodgkin Research Fellowship (DH150187) and by a European Research Council (ERC) Starting Grant (UNITY 852993).

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