Glucose and lactate metabolism by Actinomyces naeslundii

Abstract

Actinomyces are among the predominant bacteria in the oral microflora. This review discusses the glucose and lactate metabolism of Actinomyces naeslundii and its ecological significance in dental plaque. This bacterium has the Embden-Meyerhof-Parnas (EMP) pathway as the main route to degrade glucose. The EMP pathway-derived metabolic intermediates, phosphoenolpyruvate (PEP) and pyruvate, are further converted into different end-products, depending on the environment. Under anaerobic conditions in the absence of bicarbonate, the pyruvate is converted into lactate by a lactate dehydrogenase. In the presence of bicarbonate, the PEP is combined with bicarbonate and then converted into succinate through the succinate pathway, while the pyruvate is converted into formate and acetate through the pyruvate formate-lyase pathway. Under aerobic conditions, the pyruvate liberates acetate and CO2 through a pathway initiated by a pyruvate dehydrogenase. A. naeslundii strains also degrade lactate, aerobically, to acetate and CO2 through the conversion of lactate into pyruvate by a NAD-independent lactate dehydrogenase. These strains also synthesize glycogen from a glycolytic intermediate, glucose 6-phosphate. Besides atmospheric conditions and bicarbonate, the intracellular reduction-oxidation potential, carbohydrate concentration, and environmental pH also modulate the metabolism of A. naeslundii. Some of the phosphorylating enzymes involved in A. naeslundii metabolism--e.g., GTP/polyphosphate (PPn)-dependent glucokinase, pyrophosphate (PPi)-dependent phosphofructokinase, UDP-glucose pyrophosphorylase, and GDP/IDP-dependent PEP carboxykinase--are unique to A. naeslundii and have not been found in other oral bacteria. The utilization of PPn and PPi as phosphoryl donors, together with glycogen synthesis and lactate utilization, could contribute to the efficient energy metabolism found in A. naeslundii. Through this flexible and efficient metabolic capacity, A. naeslundii can adapt to fluctuating environments and compete with other bacteria in dental plaque. Further, this bacterium may modify the dental plaque environment and promote the microbial population shifts in dental plaque.