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

Ammonia oxidation is the first and rate-limiting step in nitrification and is dominated by two distinct groups of microorganismsin soil: ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB). AOA are often more abundant than AOBand 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 atnear-neutral pH when grown in standard laboratory culture. Although a number of mechanisms have been demonstrated toenable neutrophilic AOB growth at low pH in the laboratory, these have not been demonstrated in soil, and the recent cultivationof the obligately acidophilic ammonia oxidizer “Candidatus Nitrosotalea devanaterra” provides a more parsimonious explanationfor 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 essentialfor 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 mechanismsabsent in neutrophilic AOA. Analysis of mRNA revealed that candidate genes encoding the proposed homeostasis mechanismswere 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 andidentifies potential mechanisms enabling this unique phenotype for future biochemical characterization