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The role of carbon dioxide in glucose metabolism of Bacteroides fragilis

Abstract

The effect of CO2 concentration on growth and glucose fermentation of Bacteroides fragilis was studied in a defined mineral medium. Batch culture experiments were done in closed tubes containing CO2 concentrations ranging from 10% to 100% (with appropriate amounts of bicarbonate added to maintain the pH at 6.7). These experiments revealed that CO2 had no influence on growth rate or cell yield when the CO2 concentration was above 30% CO2 (minimum available CO2−HCO -3 , 25.5 mM), whereas a slight decrease in these parameters was observed at 20% and 10% CO2 (available CO2−HCO -3 , 17 and 8.5 mM, respectively). If CO2−HCO -3 concentrations were below 10 mM, the lag phase lengthened and a decrease in maximal growth rate and cell yield were observed. The amount of acetate made decreased, while d-lactate concentration increased. A net production of CO2 allowed growth under conditions of extremely low concentrations of added CO2.

When B. fragilis was grown in continuous culture with 100% CO2 or 100% N2, the dilution rate influenced the concentrations of acetate, succinate, propionate, d-lactate, l-malate and formate formed. Decreasing the dilution rate favored propionate and acetate production under both conditions. When the organism was grown with 100% N2, the amount of propionate formed was greater than the amount of succinate formed at all dilution rates. Except at slow dilution rates the reverse was true when 100% CO2 was used. B. fragilis was unable to grow at dilution rates faster than 0.154 h-1 when grown with 100% N2; the Y maxglc was 67.9 g DW cells/mol glucose and m s was 0.064 mmol glucose/g DW·h. If the gas atmosphere was 100% CO2 the organism was washed out of the culture when the dilution rate exceeded 0.38 h-1; the Y maxglc was 59.4 g DW cells/mol glucose and m s was 0.094 mmol glucose/g DW·h.

Measurement of the phosphoenolpyruvate (PEP) carboxykinase (E.C. 4.1.1.49) with whole, permeabilized cells of B. fragilis showed an increase of specific enzyme activity with decreasing CO2 concentrations. The mechanisms used by B. fragilis to adjust to low levels of CO2 are discussed.

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References

  • Boehringer, Mannheim (1980) Enzymatische Analyse für die Lebensmittelchemie

  • Caldwell DR, Keeney M, Soest PJ van (1969) Effects of carbon dioxide on growth and maltose fermentation by Bacteroides amylophilus. Bacteriol 98:668–676

    Google Scholar 

  • Carlsson J, Griffith CJ (1974) Fermentation products and bacterial yields in glucose-limited and nitrogen-limited cultures of streptococci. Arch Oral Biol 19:1105–1109

    Google Scholar 

  • Decker K, Jungermann K, Thauer RK (1970) Energy production in anaerobic organisms. Angew Chem Internat Edit 9:138–158

    Google Scholar 

  • Dehority BA (1971) Carbon dioxide requirement of various species of rumen bacteria. J Bacteriol 105:70–76

    Google Scholar 

  • DeVries W, Kapteijn WMC, Beek EG van der, Stouthamer AH (1970) Molar growth yields and fermentation balances of Lactobacillus casei L3 in batch cultures and in continuous cultures. J Gen Microbiol 63:333–345

    Google Scholar 

  • Dimroth P (1982a) Purification of the sodium transport enzyme oxaloacetate decarboxylase by affinity chromatography on avidinsepharose. FEMS Letts 141:59–62

    Google Scholar 

  • Dimroth P (1982b) The generation of an electrochemical gradient of sodium ions upon decarboxylation of oxaloacetate by the membrane-bound and Na+-activated oxaloacetate decarboxylase from Klebsiella aerogenes. Eur J Biochem 121:443–449

    Google Scholar 

  • Dowell VR, Lombard GL (1981) Pathogenic members of the genus Bacteroides. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes. Springer Berlin Heidelberg New York, pp 1425–1449

    Google Scholar 

  • Garvie EI (1980) Bacterial lactate dehydrogenases. Microbiol Reviews 44:106–139

    Google Scholar 

  • Hobson PN, Summers R (1967) The continuous culture of anaerobic bacteria. J Gen Microbiol 47:53–65

    Google Scholar 

  • Holdeman LV, Good IJ, Moore WEC (1976) Human fecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl Environ Microbiol 31:359–375

    Google Scholar 

  • Hopgood MF, Walker DJ (1967a) Succinic acid production by rumen bacteria. I. Isolation and metabolism of Ruminococcus flavefaciens. Aust J Biol Sci 20:165–182

    Google Scholar 

  • Hopgood MF, Walker DJ (1967b) Succinic acid production by rumen bacteria. II. Radioisotope studies on succinate production by Ruminococcus flavefaciens. Aust J Biol Sci 20:183–192

    Google Scholar 

  • Hopgood MF, Walker DJ (1969) Succinic acid production by rumen bacteria. III. Enzymic studies on the formation of succinate by Ruminococcus flavefaciens. Aust J Biol Sci 22:1413–1424

    Google Scholar 

  • Hungate RE (1966) The rumen and its microbes. Academic Press, New York London

    Google Scholar 

  • Hungate RE (1969) A roll tube method for cultivation of strict anaerobes. In: Norris JR, Ribbons DW (eds) Methods in microbiology, vol III. Academic Press, New York London, pp 117–132

    Google Scholar 

  • Jarvis BDW, Henderson C, Asmundson RV (1978) The role of carbonate in the metabolism of glucose by Butyrivibrio fibrisolvens. J Gen Microbiol 105:287–295

    Google Scholar 

  • Kornberg HL, Reeves RE (1972) Correlation between hexose transport and phosphotransferase activity in Escherichia coli. Biochem J 126:1241–1243

    Google Scholar 

  • Kotarski SF, Salyers AA (1981) Effect of long generation times on growth of Bacteroides thetaiotaomicron in carbohydrate-limited continuous culture. J Bacteriol 146:853–860

    Google Scholar 

  • Kröger A (1980) Bacterial electron transport to fumarate. In: Knowles CJ (ed) Diversity of bacterial respiratory systems. CRC Press, Inc., Boca Raton, Florida, pp 2–17

    Google Scholar 

  • Lang E, Lang H (1972) Spezifische Farbreaktion zum direkten Nachweis der Ameisensäure. Fresenius Z Anal Chem 260:8–10

    Google Scholar 

  • Macy JM (1981) Nonpathogenic members of the genus Bacteroides. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes. Springer Berlin Heidelberg New York pp 1450–1463

    Google Scholar 

  • Macy JM, Probst I (1979) The biology of gastrointestinal bacteroides. Ann Rev Microbiol 33:561–594

    Google Scholar 

  • Moore WEC, Holdeman LV (1974) Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl Microbiol 27:961–979

    Google Scholar 

  • Pettipher GL, Latham MJ (1979) Production of enzymes degrading plant cell walls and fermentation of cellobiose by Ruminococcus flavefaciens in batch and continuous culture. J Gen Microbiol 110:29–38

    Google Scholar 

  • Pirt SJ (1965) The maintenance energy of bacteria in growing cultures. Proc Royal Soc B 163:224–231

    Google Scholar 

  • Pirt SJ (1975) Principles of microbe and cell cultivation. Blackwell Scientific Publications, Oxford London Edinburgh Melbourne

    Google Scholar 

  • Repaske R, Clayton MA (1978) Control of Escherichia coli growth by CO2. J Bacteriol 135:1162–1164

    Google Scholar 

  • Repaske R, Ambrose CA, Repaske AC, De Lacy ML (1971) Bicarbonate requirement for elimination of the lag period of Hydrogenomonas eutropha. J Bacteriol 107:712–717

    Google Scholar 

  • Repaske R, Repaske AC, Mayer RD (1974) Carbon dioxide control of lag period and growth of Streptococcus sanguis. J Bacteriol 117:652–659

    Google Scholar 

  • Russell JB, Baldwin RL (1979) Comparison of maintenance energy expenditures and growth yields among several rumen bacteria grown on continuous culture. Appl Environ Microbiol 37:537–543

    Google Scholar 

  • Schmidt K, Liaanen-Jensen S, Schlegel HG (1963) Die Carotinoide der Thiorhodaceae. Arch Mikrobiol 46:117–126

    Google Scholar 

  • Stouthamer AH (1969) Determination and significance of molar growth yields. In: Norris JR, Ribbons DW (eds) Methods in microbiology, vol I. Academic Press, New York London, pp 629–663

    Google Scholar 

  • Thomas TD, Ellwood DC, Longyear VMC (1979) Change from homoto heterolactic fermentation by Streptococcus lactis resulting from glucose limitation in anaerobic chemostat cultures. J Bacteriol 138:109–117

    Google Scholar 

  • Umbreit WW, Burris RH, Stauffer JF (1972) Manometric and biochemical techniques, fifth edition. Burgess Publishing Company, Minneapolis, Minnesota, pp 20–29

    Google Scholar 

  • Wright DE (1960) The metabolism of carbon dioxide by Streptococcus bovis. J Gen Microbiol 22:713–725

    Google Scholar 

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Caspari, D., Macy, J.M. The role of carbon dioxide in glucose metabolism of Bacteroides fragilis . Arch. Microbiol. 135, 16–24 (1983). https://doi.org/10.1007/BF00419476

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Key words

  • CO2
  • Glucose metabolism
  • Bacteroides fragilis
  • Continuous culture
  • Maximum-growth yield
  • Maintenance
  • PEP carboxykinase