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

Abstract

Autotrophic ammonia oxidation is performed by two distinct groups of microorganisms: ammonia-oxidising archaea (AOA) and ammonia-oxidising bacteria (AOB). AOA outnumber their bacterial counterparts in many soils, at times by several orders of magnitude, but 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 influence the favoured localisation of ammonia oxidisers within the soil and the structure of ammonia-oxidising communities in terrestrial ecosystems.

Keywords: acidic soil; ammonia-oxidising archaea; autotrophy; low pH; mixotrophy; nitrification.