Energy metabolism of Actinobacillus actinomycetemcomitans during anaerobic and microaerobic growth in low- and high-potassium continuous culture

Abstract

Actinobacillus actinomycetemcomitans, a member of the gamma subclass of the Proteobacteria, has been implicated as the agent responsible for human periodontitis. In this study, A. actinomycetemcomitans 301-b was grown in fructose-limited chemostat cultures under anaerobic [redox potential (E h )TN400 mV] and microaerobic (E h lN200 mV) conditions to characterize its energy metabolism. Effects of K M and Na M on growth and metabolism were also examined. In a control medium containing 52 mM K M and 24 mM Na M , the molar growth yield on fructose (Y fructose ) of microaerobic cultures was 13 times higher than the yield of anaerobic cultures at D a 010 h N1 , but the difference in the Y fructose between microaerobic and anaerobic cultures decreased at D S 010 h N1 . When the ATP yield from fermentation was estimated from the amounts of fructose consumed and acetate formed, the value of the microaerobic culture (249 mol ATP produced per mol fructose consumed) was lower than the anaerobic value [313 mol ATP (mol fructose) N1 ]. Therefore, ATP production from fermentation could not account for the increase in the Y fructose at D a 010 h N1 and thus additional ATP was expected to be generated via respiration. Assuming that the Y ATP (g cells formed per mol ATP synthesized) was similar between anaerobic and microaerobic cultures, the estimated ATP yield from respiration was between 12 and 20 mol ATP (mol fructose) N1 below D l 010 h N1 and decreased to 03 mol ATP (mol fructose) N1 when D was increased to 019 h N1 . Such growth-rate-dependent decreases in the Y fructose and the estimated ATP production from respiration were also observed in a highNa M (52 mM K M and 106 mM Na M ) culture but not in a high-K M (81 mM K M and 24 mM Na M ) culture. In the high-K M culture, the microaerobic Y fructose was 14-20 times higher than the anaerobic value and the respiration-derived ATP yield was estimated to be between 12 and 19 mol ATP (mol fructose) N1 over a wide range of dilution rate. These results suggest that higher concentrations of extracellular K M are required for the respiration to occur in rapidly growing cells of A. actinomycetemcomitans.

Setup of an In Vitro Test System for Basic Studies on Biofilm Behavior of Mixed-Species Cultures with Dental and Periodontal Pathogens

“…The tendency of such strains to develop monolayers of viable cells for extended incubation periods has not been described so far. In general A. actinomycetemcomitans is known for its dependence on K + ion concentration [35], slow growth rate, and limited carbon catabolic capabilities [36], which could possibly explain our observations with this species.…”

A Novel Exclusion Mechanism for Carbon Resource Partitioning in Aggregatibacter actinomycetemcomitans

“…Two of these energy sources (glucose and lactate) are commonly found at high levels (approximately 1 to 5 mM) (28), while the others are found at low micromolar levels in crevicular fluid and/or plasma (28,41). We chose to focus on A. actinomycetemcomitans growth using glucose and lactate since they are the most prevalent in vivo and fructose since it is a well-studied PTS-transported carbohydrate present at low levels in vivo (16,25,(29)(30)(31). To examine growth using these in vivo relevant substrates, we utilized a CDM supplemented with these substrates as sole energy sources.…”

Potassium Channel-blockers as Therapeutic Agents to Interfere with Bone Resorption of Periodontal Disease

“…This has been suggested to be due to higher numbers of degenerating epithelial cells, connective tissue, and blood cells liberating their intracellular contents, and hence contributing to increasing the K + concentration of the exudates (Bang et al, 1973). The increased K + concentration in periodontal lesion sites, together with moderate levels of oxygen tension, appears to constitute conditions favorable for the growth of Actinobacillus actinomycetemcomitans (Ohta et al, 2001), since high concentrations of extracellular K + are required for respiration to occur in rapidly growing bacteria.…”