Nitrogen metabolism in the picoalga Pelagomonas calceolata: disentangling cyanate lyase function under different nutrient conditions.

Abstract

Cyanate (OCN-) is potentially an important organic nitrogen source in aquatic environments given the prevalence and activity of cyanate lyase genes in microalgae. However, the conditions under which these genes are expressed and the actual capacity of microalgae to assimilate cyanate remain underexplored. Here, we studied the nitrogen metabolism of the cosmopolitan picoalga Pelagomonas calceolata (Pelagophyceae, Stramenopiles) in environmental metatranscriptomes and transcriptomes from culture experiments under different nitrogen sources and concentrations. We observed that cyanate lyase is over-expressed in nitrate-poor oceanic regions, suggesting that cyanate is an important molecule contributing to the persistence of P. calceolata in oligotrophic environments. In the laboratory, we confirmed that this gene is over-expressed in low-nitrate medium together with several genes involved in nitrate recycling from endogenous molecules. Non-axenic cultures of P. calceolata were capable of growing on various nitrogen sources, including nitrate, urea and cyanate, but not ammonium. RNA sequencing of these cultures revealed that cyanate lyase was under-expressed in the presence of cyanate, indicating that this gene in not involved in the catabolism of extracellular cyanate to ammonia. Conversely, axenic P. calceolata cultures were not able to grow on cyanate, suggesting that the bacterial community consumes cyanate and provides an available form of nitrogen for growth of the alga. Based on environmental datasets and laboratory experiments, we propose that cyanate lyase is important in nitrate-poor environments to reduce the toxicity of intracellular cyanate produced by endogenous nitrogenous compound recycling, rather than being used to metabolise imported extracellular cyanate as an alternative nitrogen source.