Remodelling of carbon metabolism during sulfoglycolysis in Escherichia coli

Abstract

Sulfoquinovose (SQ) is a major metabolite in the global sulfur cycle produced by nearly all photosynthetic organisms. One of the major pathways involved in the catabolism of SQ in bacteria, such as Escherichia coli, is a variant of the glycolytic Embden-Meyerhof-Parnas (EMP) pathway termed the sulfoglycolytic EMP (sulfo-EMP) pathway, which leads to consumption of three of the six carbons of SQ and excretion of 2,3-dihydroxypropanesulfonate (DHPS). Comparative metabolite profiling of aerobically Glc-grown and SQ-grown E. coli was undertaken to identify the metabolic consequences of switching from glycolysis to sulfoglycolysis. Sulfoglycolysis was associated with the diversion of triose-phosphates to synthesize sugar phosphates (gluconeogenesis), and an unexpected accumulation of trehalose and glycogen storage carbohydrates. Sulfoglycolysis was also associated with global changes in central carbon metabolism, as indicated by changes in levels of intermediates in the tricarboxylic acid (TCA) cycle, the pentose phosphate pathway (PPP), polyamine metabolism, pyrimidine metabolism and many amino acid metabolic pathways. Upon entry into stationary phase and depletion of SQ, E. coli utilize their glycogen, indicating a reversal of metabolic fluxes to allow glycolytic metabolism. ImportanceThe sulfosugar sulfoquinovose is estimated to be produced on a scale of 10 billion tonnes per annum, making it a major organosulfur species in the biosulfur cycle. Microbial degradation of sulfoquinovose through sulfoglycolysis allows utilization of its carbon content and contributes to biomineralization of its sulfur. However, the metabolic consequences of microbial growth on sulfoquinovose are unclear. We use metabolomics to identify the metabolic adaptations that Escherichia coli undergoes when grown on sulfoquinovose versus glucose. This revealed increased flux into storage carbohydrates through gluconeogenesis, and reduced flux of carbon into the TCA cycle and downstream metabolism. These changes are relieved upon return to stationary phase growth and reversion to glycolytic metabolism. This work provides s new insights into the metabolic consequences of microbial growth on an abundant sulfosugar.