Identifying Potential Mechanisms Enabling Acidophily in the Ammonia-Oxidizing Archaeon “Candidatus Nitrosotalea devanaterra”

Laura E. Lehtovirta-Morley*, Luis A. Sayavedra-Soto, Nicolas Gallois, Stefan Schouten, Lisa Y. Stein, James I. Prosser, Graeme W. Nicol

*Corresponding author for this work

Research output: Contribution to journalArticle

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Abstract

Ammonia oxidation is the first and rate-limiting step in nitrification and is dominated by two distinct groups of microorganisms in soil: ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB). AOA are often more abundant than AOB and dominate activity in acid soils. The mechanism of ammonia oxidation under acidic conditions has been a long-standing paradox. While high rates of ammonia oxidation are frequently measured in acid soils, cultivated ammonia oxidizers grew only at near-neutral pH when grown in standard laboratory culture. Although a number of mechanisms have been demonstrated to enable neutrophilic AOB growth at low pH in the laboratory, these have not been demonstrated in soil, and the recent cultivation of the obligately acidophilic ammonia oxidizer "Candidatus Nitrosotalea devanaterra" provides a more parsimonious explanation for the observed high rates of activity. Analysis of the sequenced genome, transcriptional activity, and lipid content of "Ca. Nitrosotalea devanaterra" reveals that previously proposed mechanisms used by AOB for growth at low pH are not essential for archaeal ammonia oxidation in acidic environments. Instead, the genome indicates that "Ca. Nitrosotalea devanaterra" contains genes encoding both a predicted high-affinity substrate acquisition system and potential pH homeostasis mechanisms absent in neutrophilic AOA. Analysis of mRNA revealed that candidate genes encoding the proposed homeostasis mechanisms were all expressed during acidophilic growth, and lipid profiling by high-performance liquid chromatography-mass spectrometry (HPLC-MS) demonstrated that the membrane lipids of "Ca. Nitrosotalea devanaterra" were not dominated by crenarchaeol, as found in neutrophilic AOA. This study for the first time describes a genome of an obligately acidophilic ammonia oxidizer and identifies potential mechanisms enabling this unique phenotype for future biochemical characterization.

Original languageEnglish
Pages (from-to)2608-2619
Number of pages12
JournalApplied and Environmental Microbiology
Volume82
Issue number9
Early online date19 Feb 2016
DOIs
Publication statusPublished - 1 May 2016

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acidophily
Archaea
Ammonia
ammonia
Soil
oxidants
oxidation
Bacteria
bacterium
genome
lipid
bacteria
homeostasis
Genome
acid soil
acid soils
Homeostasis
Growth

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Food Science
  • Biotechnology
  • Ecology

Cite this

Identifying Potential Mechanisms Enabling Acidophily in the Ammonia-Oxidizing Archaeon “Candidatus Nitrosotalea devanaterra”. / Lehtovirta-Morley, Laura E.; Sayavedra-Soto, Luis A.; Gallois, Nicolas; Schouten, Stefan; Stein, Lisa Y.; Prosser, James I.; Nicol, Graeme W.

In: Applied and Environmental Microbiology, Vol. 82, No. 9, 01.05.2016, p. 2608-2619.

Research output: Contribution to journalArticle

Lehtovirta-Morley, Laura E. ; Sayavedra-Soto, Luis A. ; Gallois, Nicolas ; Schouten, Stefan ; Stein, Lisa Y. ; Prosser, James I. ; Nicol, Graeme W. / Identifying Potential Mechanisms Enabling Acidophily in the Ammonia-Oxidizing Archaeon “Candidatus Nitrosotalea devanaterra”. In: Applied and Environmental Microbiology. 2016 ; Vol. 82, No. 9. pp. 2608-2619.
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