Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

Ammonia-oxidizing archaea (AOA) constitute a considerable fraction of microbial biomass in the global ocean, comprising 20-40% of the ocean’s prokaryotic plankton and thus play an important role in global nitrogen cycle. However, it remains enigmatic to what extent these chemolithoautotrophic archaea are releasing dissolved organic matter (DOM). A combination of targeted and untargeted metabolomics was used to characterise the exometabolomes of three model AOA strains of the Nitrosopumilus genus. Furthermore, we compared the composition of intra- and extracellular dissolved free amino acids (DFAA). Our results indicate that marine AOA exude a suite of organic compounds with potentially varying reactivity, dominated by nitrogen-containing compounds. A significant fraction of the released DOM consisted of labile compounds, which typically limit prokaryotic heterotrophic activity in open ocean waters, including amino acids, thymidine and B vitamins. In growing Nitrosopumilus cultures, hydrophobic amino acids were likely released as a result of passive diffusion corresponding to ammonia oxidation activity, while glycine was continuously released at high rates. Our results suggest that AOA release several ecologically and biochemically relevant metabolites, potentially fueling heterotrophic prokaryotes in the ocean.