Decoding Icy Metabolism: Flux Topology of a Psychrophilic Extremophile

Recent advancements in the mass spectrometry and system biology tools such as RNA-Seq have allowed for the precise characterization of microorganisms’ metabolic functions. Representative species from many extreme environments have been characterized, from mesophilic to thermophilic and acidophilic organisms. Even though the volume of cold-temperature environments dwarfs that of other habitats, characterization of cold-adapted microorganism has remained relatively unexplored.

Here, we present the characterization of the marine psychrophilic extremophile, Colwellia psychrerythraea 34H, which grows at 0°C. We experimentally determined the biomass composition as well as the proteinogenic and lipid profiles of the bacteria. We used steady state ¹³C-fingerprinting and ¹³C-metbaolic flux analysis in conjugation with ¹³C-dynamic labeling experiments to elucidate the central metabolic pathways of 34H grown on glucose and lactate. In tandem, we performed RNA-Seq analysis at icy temperature and room temperature to determine the global rearrangement of 34H’s metabolism. We also used flux balance analysis to understand the cellular ‘objective function’ of 34H by comparing the computationally predict fluxes to the experimental determined fluxes. Finally, we used thermodynamic comparisons to explore the driving forces that may have led to the prevalence of the Entner–Doudoroff (ED) pathway among marine bacteria.