Temperature-dependent growth kinetics of Escherichia coli ML 30 in glucose-limited continuous culture

Detailed comparison of growth kinetics at temperatures below and above the optimal temperature was carried out with Escherichia coli ML 30 (DSM 1329) in continuous culture. The culture was grown with glucose as the sole limiting source of carbon and energy (100 mg liter(-1) in feed medium), and the resulting steady-state concentrations of glucose were measured as a function of the dilution rate at 17.4, 28.4, 37, and 40 degrees C. The experimental data could not be described by the conventional Monod equation over the entire temperature range, but an extended form of the Monod model [mu = mu(max) x (s - s(min))/(Ks + s - s(min))], which predicts a finite substrate concentration at 0 growth rate (s(min)), provided a good fit. The two parameters mu(max) and s(min) were temperature dependent, whereas, surprisingly, fitting the model to the experimental data yielded virtually identical Ks values (approximately 33 microg liter(-1)) at all temperatures. A model that describes steady-state glucose concentrations as a function of temperature at constant growth rates is presented. In similar experiments with mixtures of glucose and galactose (1:1 mixture), the two sugars were utilized simultaneously at all temperatures examined, and their steady-state concentrations were reduced compared with to growth with either glucose or galactose alone. The results of laboratory-scale kinetic experiments are discussed with respect to the concentrations observed in natural environments.

[1]  M H Zwietering,et al.  Modelling bacterial growth of Listeria monocytogenes as a function of water activity, pH and temperature. , 1993, International journal of food microbiology.

[2]  D. Söndgerath,et al.  Parameter Estimation in Ecology: The Link between Data and Models , 1990 .

[3]  F. Neidhardt,et al.  Levels of major proteins of Escherichia coli during growth at different temperatures , 1979, Journal of bacteriology.

[4]  N. W. F. Kossen,et al.  The influence of temperature on the maximum specific growth rate of Klebsiella pneumoniae , 1981 .

[5]  C. G. Sinclair,et al.  Temperature relationship in continuous culture , 1971 .

[6]  K van't Riet,et al.  Modeling of bacterial growth as a function of temperature , 1991, Applied and environmental microbiology.

[7]  J Olley,et al.  Relationship between temperature and growth rate of bacterial cultures , 1982, Journal of bacteriology.

[8]  M R Adams,et al.  Modelling the effect of pH, acidulant and temperature on the growth rate of Yersinia enterocolitica. , 1991, The Journal of applied bacteriology.

[9]  M. K. Shaw,et al.  Fatty Acid Composition of Escherichia coli as a Possible Controlling Factor of the Minimal Growth Temperature , 1965, Journal of bacteriology.

[10]  T. Egli,et al.  The growth of Escherichia coli in glucose-limited chemostat cultures: a re-examination of the kinetics. , 1994, Biochimica et biophysica acta.

[11]  J. A. Robinson,et al.  Determining microbial kinetic parameters using nonlinear regression analysis. Advantages and limitations in microbial ecology , 1985 .

[12]  J. Ingraham,et al.  DAMAGE AND DEREPRESSION IN ESCHERICHIA COLI RESULTING FROM GROWTH AT LOW TEMPERATURES , 1962, Journal of bacteriology.

[13]  J P Flandrois,et al.  Convenient Model To Describe the Combined Effects of Temperature and pH on Microbial Growth , 1995, Applied and environmental microbiology.

[14]  Willi Gujer,et al.  TEMPERATURE DEPENDENCY OF MICROBIAL REACTIONS , 1979 .

[15]  R. Buchanan,et al.  The effect of incubation temperature, initial pH, and sodium chloride on the growth kinetics of Escherichia coli O157:H7 , 1992 .

[16]  R. Y. Morita,et al.  Bioavailability of energy and its relationship to growth and starvation survival in nature , 1988 .

[17]  J. S. Hough,et al.  The effect of temperature on the metabolism of baker's yeast growing on continuous culture. , 1970, Journal of general microbiology.

[18]  T. A. Roberts,et al.  The effect of sodium chloride and temperature on the rate and extent of growth of Clostridium botulinum type A in pasteurized pork slurry. , 1987, The Journal of applied bacteriology.

[19]  A. N. Stokes,et al.  Model for bacterial culture growth rate throughout the entire biokinetic temperature range , 1983, Journal of bacteriology.

[20]  M. Shuler,et al.  Predicting threshold concentrations of organic substrates for bacterial growth , 1985 .

[21]  A. Zehnder,et al.  Transformation of Low Concentrations of 3-Chlorobenzoate by Pseudomonas sp. Strain B13: Kinetics and Residual Concentrations , 1996, Applied and environmental microbiology.

[22]  S. Pirt The maintenance energy of bacteria in growing cultures , 1965, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[23]  von Meyenburg Kaspar Transport-limited growth rates in a mutant of Escherichia coli. , 1971, Journal of bacteriology.

[24]  M. Kito,et al.  Temperature-sensitive formation of the phospholipid molecular species in Escherichia coli membranes. , 1976, Biochimica et biophysica acta.

[25]  E. Ron,et al.  Growth Rate of Escherichia coli at Elevated Temperatures: Reversible Inhibition of Homoserine Trans-Succinylase , 1971, Journal of bacteriology.

[26]  James V. Beck,et al.  Parameter Estimation in Engineering and Science , 1977 .

[27]  P. Westermann,et al.  Temperature Compensation in Methanosarcina barkeri by Modulation of Hydrogen and Acetate Affinity , 1989, Applied and environmental microbiology.

[28]  D. Ratkowsky,et al.  Model for combined effect of temperature and salt concentration/water activity on the growth rate of Staphylococcus xylosus. , 1987, The Journal of applied bacteriology.

[29]  A. Downing,et al.  DETERMINATION OF KINETIC CONSTANTS FOR NITRIFYING BACTERIA IN MIXED CULTURE, WITH THE AID OF AN ELECTRONIC COMPUTER. , 1965, Journal of general microbiology.

[30]  W. Hempfling,et al.  Effects of growth temperature on yield and maintenance during glucose-limited continuous culture of Escherichia coli , 1976, Journal of bacteriology.

[31]  P. Reichert,et al.  Utility of phenomenological models for describing temperature dependence of bacterial growth , 1991, Applied and environmental microbiology.

[32]  A. G. Marr,et al.  Effect of Nutrient Concentration on the Growth of Escherichia coli , 1971, Journal of bacteriology.

[33]  J. Monod,et al.  Recherches sur la croissance des cultures bactériennes , 1942 .

[34]  R. Wallace,et al.  Maintenance coefficients and rates of turnover of cell material in Escherichia coli ML308 at different growth temperatures , 1986 .

[35]  G. Hamer,et al.  Heat shock gene expression in continuous cultures of Escherichia coli. , 1992, Journal of biotechnology.

[36]  K. Hellingwerf,et al.  Thermodynamics of growth. Non-equilibrium thermodynamics of bacterial growth. The phenomenological and the mosaic approach. , 1982, Biochimica et biophysica acta.

[37]  S. J. Pirt,et al.  Principles of microbe and cell cultivation , 1975 .

[38]  M. H. Zwietering,et al.  Modeling of Bacterial Growth with Shifts in Temperature , 1994, Applied and environmental microbiology.

[39]  B. Averhoff,et al.  Identification of the transcriptional activator pobR and characterization of its role in the expression of pobA, the structural gene for p-hydroxybenzoate hydroxylase in Acinetobacter calcoaceticus , 1993, Journal of bacteriology.

[40]  M. Zwietering,et al.  Modelling Bacterial Growth of Lactobacillus curvatus as a Function of Acidity and Temperature , 1995, Applied and environmental microbiology.

[41]  J. Ingraham,et al.  EFFECT OF THE TEMPERATURE OF GROWTH OF ESCHERICHIA COLI ON THE FORMATION OF β-GALACTOSIDASE , 1964 .

[42]  J P Flandrois,et al.  An unexpected correlation between cardinal temperatures of microbial growth highlighted by a new model. , 1993, Journal of theoretical biology.