Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats

Ammonia oxidation in marine and terrestrial ecosystems plays a pivotal role in the cycling of nitrogen and carbon. Recent discoveries have shown that ammonia-oxidizing archaea (AOA) are both abundant and diverse in these systems, yet very little is known about their physiology. Here we report a physiological analysis of a novel low-salinity-type AOA enriched from the San Francisco Bay estuary, Candidatus Nitrosoarchaeum limnia strain SFB1. N. limnia has a slower growth rate than Nitrosopumilus maritimus and Nitrososphaera viennensis EN76, the only pure AOA isolates described to date, but the growth rate is comparable to the growth of marine AOA enrichment cultures. The growth rate only slightly decreased when N. limnia was grown under lower-oxygen conditions (5.5 % oxygen in the headspace). Although N. limnia was capable of growth at 75 % of seawater salinity, there was a longer lag time, incomplete oxidation of ammonia to nitrite, and slower overall growth rate. Allylthiourea (ATU) only partially inhibited growth and ammonia oxidation by N. limnia at concentrations known to completely inhibit bacterial ammonia oxidation. Using electron microscopy, we confirmed the presence of flagella as suggested by various flagellar biosynthesis genes in the N. limnia genome. We demonstrate that N. limnia is representative of a low-salinity estuarine AOA ecotype and that more than 85 % of its proteins have highest identity to other coastal and estuarine metagenomic sequences. Our findings further highlight the physiology of N. limnia and help explain its ecological adaptation to low-salinity niches.