Cyanate as an energy source for nitrifiers

Abstract

Ammonia-and nitrite-oxidizers are collectively responsible for the aerobic oxidation of ammonia via nitrite to nitrate and play essential roles for the global biogeochemical nitrogen cycle. The physiology of these nitrifying microbes has been intensively studied since the first experiments of Sergei Winogradsky more than a century ago. Urea and ammonia are the only recognized energy sources that promote the aerobic growth of ammonia-oxidizing bacteria and archaea. Here we report the aerobic growth of a pure culture of the ammonia-oxidizing thaumarchaeote Nitrososphaera gargensis 1 on cyanate as the sole source of energy and reductant, the first organism known to do so. Cyanate, which is a potentially important source of reduced nitrogen in aquatic and terrestrial ecosystems 2 , is converted to ammonium and CO 2 by this archaeon using a cyanase that is induced upon addition of this compound. Within the cyanase gene family, this cyanase is a member of a distinct clade that also contains cyanases of nitrite-oxidizing bacteria of the genus Nitrospira. We demonstrate by co-culture experiments that these nitrite-oxidizers supply

Physiology, Biochemistry, and Applications of F420- and Fo-Dependent Redox Reactions

“…Comparative genomics indicate that the genes required for F 420 biosynthesis are also distributed in the Thaumarchaeota, Aigarchaeota, Geoarchaeota, Bathyarchaeota, and Lokiarchaeota (138)(139)(140)(141)(142). The absorbance spectra of single cells of the ammonia-and cyanate-oxidizing thaumarchaeon Nitrososphaera gargensis are also consistent with the presence of F 420 (143,144). It is unclear whether F 420 is pro- duced by Crenarchaeota; while the cofactor was reported to be present at low levels in representatives of the Sulfolobus and Thermoplasma (20), the genomes of these organisms suggest that in fact they lack the capacity to synthesize this deazaflavin by any currently understood biosynthetic mechanism.…”

Integrated metabolism in sponge–microbe symbiosis revealed by genome-centered metatranscriptomics

“…Genomic analysis of several Thaumarchaea species revealed the presence of genes related to transport, production and degradation of urea (Palatinszky et al, 2015). Urea can be used by Thaumarchaeota members as source of ammonia, as shown by biochemical assays of cultivated species (Lehtovirta-Morley et al, 2016), and as carbon source, as inferred from 14 C-labeled urea incorporation of prokaryotic communities of Artic waters (Alonso-Saez et al, 2012).…”

“…Cyanate lyase decomposes cyanate to CO 2 and ammonia in a reaction dependent of bicarbonate (Johnson and Anderson, 1987). Its activity was described in N. moscoviensis and its proposed biological roles include nitrogen assimilation, cyanate detoxification and energy acquisition (Anderson et al, 1990;Palatinszky et al, 2015). The cya gene was localized downstream from two genes encoding for proteins of the formate/nitrite transporter family (TPM av 513-904) (Supplementary Figure S9).…”

“…We did not find genomic evidence for the internal production of urea by CcNi, such as genes encoding for agmatinase or arginase. Because nitrite-oxidizing bacteria encode urea-producing enzymes (Palatinszky et al, 2015), the possibility of Nitrospira-like genes encoding for agmatinase or arginase to be expressed in C. concentrica was investigated. Transcripts encoding for sequences similar to agmatinase or arginase were found in the metatranscriptome of C. concentrica (Díez-Vives et al, 2016), but none of them were related to Nitrospira (Supplementary Information; Supplementary Table S4).…”

“…Nitrification, a process in which the oxidation of ammonia is coupled with the oxidation of nitrite, is a common Integrated metabolism in sponge-microbe symbiosis L Moitinho-Silva et al theme in sponge microbiology, being the subject of many studies (Taylor et al, 2007). Based on the use of urea and cyanate as indirect sources of ammonia in nitrification carried out by co-cultures of Nitrospira and ammonia-oxidizing bacteria (Koch et al, 2015;Palatinszky et al, 2015) and the expression profile of CcNi and CcThau, we propose that these compounds should be considered when modeling nitrification in marine sponges.…”