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

International audienceAmmonia oxidation is the first and rate-limiting step in nitrification and is dominated by two distinct groups of microorganisms in soil: ammonia-oxidising archaea (AOA) and bacteria (AOB). AOA are often more abundant than AOB, and dominate activity in acid soils. The mechanism of ammonia oxidation in acidic conditions has been a long-standing paradox. While high rates of ammonia oxidation are frequently measured in acid soils, cultivated ammonia oxidisers only grew 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 oxidiser ‘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. N. 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. N. 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 for the proposed homeostasis mechanisms were all expressed during acidophilic growth, and lipid profiling by HPLC-MS demonstrated that the membrane lipids of ‘Ca. N. devanaterra’ were not dominated by crenarchaeol, as found in neutrophilic AOA. This study describes the first genome of an obligately acidophilic ammonia oxidiser and identifies potential mechanisms enabling this unique phenotype for future biochemical characterisation