Production and Excretion of Polyamines To Tolerate High Ammonia, a Case Study on Soil Ammonia-Oxidizing Archaeon “<italic toggle="yes">Candidatus</italic> Nitrosocosmicus agrestis”

Abstract

ABSTRACT Ammonia tolerance is a universal characteristic among the ammonia-oxidizing bacteria (AOB); in contrast, the known species of ammonia-oxidizing archaea (AOA) have been regarded as ammonia sensitive, until the identification of the genus “Candidatus Nitrosocosmicus.” However, the mechanism of its ammonia tolerance has not been reported. In this study, the AOA species “Candidatus Nitrosocosmicus agrestis,” obtained from agricultural soil, was determined to be able to tolerate high concentrations of NH3 (>1,500 μM). In the genome of this strain, which was recovered from metagenomic data, a full set of genes for the pathways of polysaccharide metabolism, urea hydrolysis, arginine synthesis, and polyamine synthesis was identified. Among them, the genes encoding cytoplasmic carbonic anhydrase (CA) and a potential polyamine transporter (drug/metabolite exporter [DME]) were found to be unique to the genus “Ca. Nitrosocosmicus.” When “Ca. Nitrosocosmicus agrestis” was grown with high levels of ammonia, the genes that participate in CO2/HCO3− conversion, glutamate/glutamine syntheses, arginine synthesis, polyamine synthesis, and polyamine excretion were significantly upregulated, and the polyamines, including putrescine and spermidine, had significant levels of production. Based on genome analysis, gene expression quantification, and polyamine determination, we propose that the production and excretion of polyamines is probably one of the reasons for the ammonia tolerance of “Ca. Nitrosocosmicus agrestis,” and even of the genus “Ca. Nitrosocosmicus.” IMPORTANCE Ammonia tolerance of AOA is usually much lower than that of the AOB, which makes the AOB rather than AOA a predominant ammonia oxidizer in agricultural soils, contributing to global N2O emission. Recently, some AOA species from the genus “Ca. Nitrosocosmicus” were also found to have high ammonia tolerance. However, the reported mechanism for the ammonia tolerance is very rare and indeterminate for AOB and for AOA species. In this study, an ammonia-tolerant AOA strain of the species “Ca. Nitrosocosmicus agrestis” was identified and its potential mechanisms for ammonia tolerance were explored. This study will be of benefit for determining more of the ecological role of AOA in agricultural soils or other environments.

Keywords

• ammonia tolerance
• ammonia-oxidizing archaea
• Nitrosocosmicus
• polyamines