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

H. Ohta, T. Inoue, K. Fukui

Research output: Contribution to journalArticle

7 Citations (Scopus)

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 (Eh) h = -200 mV) conditions to characterize its energy metabolism. Effects of K+ and Na+ on growth and metabolism were also examined. In a control medium containing 5.2 mM K+ and 24 mM Na+, the molar growth yield on fructose (Yfructose) of microaerobic cultures was 1.3 times higher than the yield of anaerobic cultures at D ≤ 0.10 h-1, but the difference in the Yfructose between microaerobic and anaerobic cultures decreased at D > 0.10 h-1. When the ATP yield from fermentation was estimated from the amounts of fructose consumed and acetate formed, the value of the microaerobic culture (2.49 mol ATP produced per mol fructose consumed) was lower than the anaerobic value [3.13 mol ATP (mol fructose)-1]. Therefore, ATP production from fermentation could not account for the increase in the Yfructose at D ≤ 0.10 h-1 and thus additional ATP was expected to be generated via respiration. Assuming that the YATP (g cells formed per mol ATP synthesized) was similar between anaerobic and microaerobic cultures, the estimated ATP yield from respiration was between 1.2 and 2.0 mol ATP (mol fructose)-1 below D = 0.10 h-1 and decreased to 0.3 mol ATP (mol fructose)-1 when D was increased to 0.19 h-1. Such growth-rate-dependent decreases in the Yfructose and the estimated ATP production from respiration were also observed in a high-Na+ (5.2 mM K+ and 106 mM Na+) culture but not in a high-K+ (81 mM K+ and 24 mM Na+) culture. In the high-K+ culture, the microaerobic Yfructose was 1.4-2.0 times higher than the anaerobic value and the respiration-derived ATP yield was estimated to be between 1.2 and 1.9 mol ATP (mol fructose)-1 over a wide range of dilution rate. These results suggest that higher concentrations of extracellular K+ are required for the respiration to occur in rapidly growing cells of A. actinomycetemcomitans.

Original languageEnglish
Pages (from-to)2461-2468
Number of pages8
JournalMicrobiology
Volume147
Issue number9
Publication statusPublished - 2001
Externally publishedYes

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Aggregatibacter actinomycetemcomitans
Fructose
Energy Metabolism
Potassium
Adenosine Triphosphate
Growth
Respiration
Fermentation
Gammaproteobacteria
Periodontitis
Oxidation-Reduction
Acetates

Keywords

  • Chemostat culture
  • Fructose metabolism
  • Microaerophile
  • Periodontopathogen
  • Potassium ion

ASJC Scopus subject areas

  • Microbiology

Cite this

Energy metabolism of Actinobacillus actinomycetemcomitans during anaerobic and microaerobic growth in low- and high- potassium continuous culture. / Ohta, H.; Inoue, T.; Fukui, K.

In: Microbiology, Vol. 147, No. 9, 2001, p. 2461-2468.

Research output: Contribution to journalArticle

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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 (Eh) h = -200 mV) conditions to characterize its energy metabolism. Effects of K+ and Na+ on growth and metabolism were also examined. In a control medium containing 5.2 mM K+ and 24 mM Na+, the molar growth yield on fructose (Yfructose) of microaerobic cultures was 1.3 times higher than the yield of anaerobic cultures at D ≤ 0.10 h-1, but the difference in the Yfructose between microaerobic and anaerobic cultures decreased at D > 0.10 h-1. When the ATP yield from fermentation was estimated from the amounts of fructose consumed and acetate formed, the value of the microaerobic culture (2.49 mol ATP produced per mol fructose consumed) was lower than the anaerobic value [3.13 mol ATP (mol fructose)-1]. Therefore, ATP production from fermentation could not account for the increase in the Yfructose at D ≤ 0.10 h-1 and thus additional ATP was expected to be generated via respiration. Assuming that the YATP (g cells formed per mol ATP synthesized) was similar between anaerobic and microaerobic cultures, the estimated ATP yield from respiration was between 1.2 and 2.0 mol ATP (mol fructose)-1 below D = 0.10 h-1 and decreased to 0.3 mol ATP (mol fructose)-1 when D was increased to 0.19 h-1. Such growth-rate-dependent decreases in the Yfructose and the estimated ATP production from respiration were also observed in a high-Na+ (5.2 mM K+ and 106 mM Na+) culture but not in a high-K+ (81 mM K+ and 24 mM Na+) culture. In the high-K+ culture, the microaerobic Yfructose was 1.4-2.0 times higher than the anaerobic value and the respiration-derived ATP yield was estimated to be between 1.2 and 1.9 mol ATP (mol fructose)-1 over a wide range of dilution rate. These results suggest that higher concentrations of extracellular K+ are required for the respiration to occur in rapidly growing cells of A. actinomycetemcomitans.",
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