Genomic evidence for the use of alternative nitrogen substrates by anammox bacteria. marine metagenome

Anaerobic ammonia oxidation (anammox) contributes substantially to total fixed nitrogen loss from the oceans, particularly in oxygen minimum zones (OMZs). Ammonium is scarce in OMZs, raising the hypothesis that other reduced nitrogen compounds may be used to generate ammonium for anammox. Recent biochemical measurements suggest that the organic nitrogen compounds urea and cyanate can support anammox in OMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonia themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria genomes, and genetic evidence for cyanate degradation by anammox bacteria is limited to a single copy of a putative cyanase homolog found in the genome of the sediment bacterium Candidatus Scalindua profunda. Here, analysis of single-cell amplified genomes (SAGs) of Ca. Scalindua arabica from the world’s largest OMZ revealed the full suite of genes for urea degradation and transport, as well as genes for cyanate degradation. Both urease and cyanase genes were transcribed in the OMZ, together with genes mediating anammox, in the anoxic core of the OMZ where anammox rates peaked. Close homologs of these genes were also detected in meta-omic datasets from other OMZs, including those of the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from diverse OMZ systems may directly use organic nitrogen-containing substrates for ammonium production to drive anammox, and potentially as a source of carbon for autotrophy, prompting a need to reevaluate chemical-microbial linkages in ocean nitrogen loss processes.