Metabolic Response of a Chemolithoautotrophic Archaeon to Carbon Limitation

Abstract

The ubiquitously distributed ammonia-oxidizing archaea generate energy from ammonia and build cell mass from inorganic carbon sources, thereby contributing to both the global nitrogen and carbon cycles. However, little is known about the regulation of their predicted core carbon metabolism. A thermodynamic model for Nitrososphaera viennensis was developed to estimate the consumption of inorganic carbon in relation to ammonia consumed for energy and was tested experimentally by growing cells in carbon-limited and excess conditions. A combined proteomic and metabolomic approach of the experimental conditions revealed distinct metabolic adaptation depending on the amount of carbon supplied, either in a catalase or pyruvate background as a reactive oxygen species scavenger. Integration of protein and metabolite dynamics revealed a cellular strategy under carbon limitation to maintain a pool of amino acids and an upregulation of proteins necessary for translation initiation to stay primed for protein synthesis. The combination of modelling and functional genomics fills gaps in the understanding of the central metabolism and its regulation in a chemolithoautotrophic, ammonia-oxidizing archaeon even in the absence of available genetic tools.