Special metabolic properties of the marine photoheterotrophic bacterium Dinoroseobacter shibae DFL 12T

Abstract

Marine bacteria face many biotic and abiotic challenges in their natural environment. These include abiotic environmental factors such as temperature, salinity and light, and biotic environmental factors such as nutrient availability and competitors. In addition, most of the factors mentioned are subject to seasonal fluctuations. The abundance of the Roseobacter group in the oceans suggests that they have adapted perfectly to the adverse conditions in their natural environment. Aiming to unravel the special metabolic properties of the Roseobacter member Dinoroseobacter shibae DFL12T especially with regard to the utilization of different carbon sources and the adaptation to changing light availability, diverse analytical experiments were conducted in the present work. Process-controlled bioreactor cultivation and metabolome analyses via GC-MS and HPLC-MS measurements have shown that the physiological and metabolic properties of D. shibae vary greatly depending on the carbon source supplied. Growth on the carboxylic acids succinate and acetate was characterized by high substrate and oxygen uptake rates and a thereof resulting high growth rate. Metabolome data showed that this was due to an efficient substrate uptake and a rapid metabolization via the ethylmalonyl-CoA (EMC) pathway (in case of acetate) and the tricarboxylic acid (TCA) cycle. Glucose, on the other hand, was metabolized via the Entner-Doudoroff pathway and glycolysis, in which reduction equivalents and ATP are produced, so that the TCA cycle operated primarily for the formation of precursors needed for other biosynthetic pathways. Furthermore, within the collaborative systems biology study a comprehensive overview on the complex adaption of D. shibae during transition from heterotrophy to photoheterotrophy was obtained. Growth in light was characterized by reduced respiration, a decreased metabolic flux through the TCA cycle and the assimilation of CO2 via an enhanced flux through the EMC pathway, which was shown to be connected to the serine metabolism in D. shibae. Adaptation to photoheterotrophy is mainly characterized by metabolic reactions caused by a surplus of reducing potential and might depend on genes located in one operon, encoding branching point enzymes of the EMC pathway, serine metabolism and the TCA cycle.