The metabolism of polar archaea: is urea playing a role?

Abstract

An annual recurrent growth of archaea in winter surface waters has been detected in polar systems. However, the sources of carbon and energy sustaining their growth remain elusive. We collected data on abundance and metabolic activity of Thaumarchaeota in Arctic and Antarctic waters by in situ single-cell analyses. The abundance of archaea grew one order of magnitude throughout the winter in Arctic waters. Yet, paradoxically, analyses by MicroAutoRadiography combined with Fluorescence In Situ Hybridization (MAR-FISH) revealed an unexpectedly low metabolic activity of Thaumarchaeota for both polar systems. Less than 5% of all thaumarchaeal cells took up leucine or bicarbonate, inconsistent with currently recognized heterotrophic and autotrophic archaeal lifestyles. To better understand how archaea obtain energy and carbon for growth, we analyzed a metagenome collected during the Arctic winter, when the Thaumarchaeota population was at its maximum of abundance (18% of cell counts). The metagenomic analysis revealed that archaeal amoA genes were abundant, indicating that polar archaea have the potential for ammonia oxidation. Furthermore, the presence of archaeal genes involved in urea transport and degradation suggests that Arctic archaea may use urea as an alternative source of ammonia, and thus energy for growth. Genes encoding ureases were also detected in Antarctic waters, confirming that urea degradation pathways are widespread among polar Thaumarchaeota, and hinting at the potential importance of urea to sustain their growth