Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds

Laura E Lehtovirta-Morley, Chaorong Ge, Jenna Ross, Huaiying Yao, Graeme W Nicol, James I Prosser

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Abstract

Autotrophic ammonia oxidation is performed by two distinct groups of microorganisms: ammonia-oxidising archaea (AOA) and ammonia-oxidising bacteria (AOB). Although AOA outnumber their bacterial counterparts in many soils, at times by several orders of magnitude, relatively little is known of their physiology due to the lack of cultivated isolates. Although a number of AOA have been cultivated from soil, Nitrososphaera viennensis was the sole terrestrial AOA in pure culture and requires pyruvate for growth in the laboratory. Here we describe isolation in pure culture and characterisation of two acidophilic terrestrial AOA representing the Candidatus genus Nitrosotalea and their responses to organic acids. Interestingly, despite their close phylogenetic relatedness, the two Nitrosotalea strains exhibited differences in physiological features, including specific growth rate, temperature preference and to an extent, response to organic compounds. In contrast to N. viennensis, both Nitrosotalea isolates were inhibited by pyruvate but their growth yield increased in the presence of oxaloacetate. This study demonstrates physiological diversity within AOA species and between different AOA genera. Different preferences for organic compounds potentially influences the favoured localisation of ammonia oxidisers within the soil and the structure of ammonia-oxidising communities in terrestrial ecosystems. This article is protected by copyright. All rights reserved.

Original languageEnglish
Pages (from-to)542-552
Number of pages11
JournalFEMS Microbiology Ecology
Volume89
Issue number3
Early online date31 Jul 2014
DOIs
Publication statusPublished - Sep 2014

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Ammonia
Archaea
Soil
Pyruvic Acid
Growth
Oxaloacetic Acid
Ecosystem
Bacteria
Temperature
Acids

Keywords

  • ammonia-oxidising archaea
  • acidic soil
  • low pH
  • mixotrophy
  • autotrophy
  • nitrification

Cite this

Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds. / Lehtovirta-Morley, Laura E; Ge, Chaorong; Ross, Jenna; Yao, Huaiying; Nicol, Graeme W; Prosser, James I.

In: FEMS Microbiology Ecology, Vol. 89, No. 3, 09.2014, p. 542-552.

Research output: Contribution to journalArticle

Lehtovirta-Morley, Laura E ; Ge, Chaorong ; Ross, Jenna ; Yao, Huaiying ; Nicol, Graeme W ; Prosser, James I. / Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds. In: FEMS Microbiology Ecology. 2014 ; Vol. 89, No. 3. pp. 542-552.
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N2 - Autotrophic ammonia oxidation is performed by two distinct groups of microorganisms: ammonia-oxidising archaea (AOA) and ammonia-oxidising bacteria (AOB). Although AOA outnumber their bacterial counterparts in many soils, at times by several orders of magnitude, relatively little is known of their physiology due to the lack of cultivated isolates. Although a number of AOA have been cultivated from soil, Nitrososphaera viennensis was the sole terrestrial AOA in pure culture and requires pyruvate for growth in the laboratory. Here we describe isolation in pure culture and characterisation of two acidophilic terrestrial AOA representing the Candidatus genus Nitrosotalea and their responses to organic acids. Interestingly, despite their close phylogenetic relatedness, the two Nitrosotalea strains exhibited differences in physiological features, including specific growth rate, temperature preference and to an extent, response to organic compounds. In contrast to N. viennensis, both Nitrosotalea isolates were inhibited by pyruvate but their growth yield increased in the presence of oxaloacetate. This study demonstrates physiological diversity within AOA species and between different AOA genera. Different preferences for organic compounds potentially influences the favoured localisation of ammonia oxidisers within the soil and the structure of ammonia-oxidising communities in terrestrial ecosystems. This article is protected by copyright. All rights reserved.

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