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Kinetics of microbial growth with mixtures of carbon sources

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Abstract

Several investigations have shown that during growth in carbon-limited chemostats the simultaneous utilisation of carbon substrates which usually provoke diauxie under batch conditions, i.e., ‘mixed substrate growth’, is probably the rule under ecologically relevant growth conditions. In contrast, the models presently available for the description of the kinetics of microbial growth are all based on the use of single substrates. Systematic studies in chemostat culture have shown that steady-state residual concentrations of individual compounds were consistently lower during mixed substrate growth than during growth with the single substrates. This effect is clearly demonstrated for the case ofEscherichia coli growing with mixtures of glucose plus galactose. The data presented indicate that the extent of reduction of steady-state residual substrate concentration is dependent on the proportions of the substrates in the mixture, the nature of substrates mixed and the regulation pattern of enzymes involved in their breakdown. If this behaviour can be shown to be typical for growth under environmental conditions, it may provide an explanation why microbes still grow relatively fast at the low substrate concentrations encountered in nature.

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Abbreviations

S0 :

Substrate concentration in medium fed to chemostat (mg L−1)

D:

Dilution rate (h−1)

DW:

Biomass dry weight (mg L−1)

μ:

Specific growth rate μmax, maximum specific growth rate (h−1)

Ks :

Monod affinity constant for substrate s, K1,2, for substrates 1, 2, respectively (mg L−1, µg L−1)

qA :

Specific consumption rate for substrate A, qtotal, total specific substrate consumption rate (mg A [mg DW]−1 h−1)

s:

Concentration of substrate in culture, sA, of substrate A (mg L−1, µg L−1)

s A :

Steady-state concentration of substrate A in chemostat,s A(100%), during growth with A only,s A(mix), during growth with mixture (mg L−1, µg L−1)

YX/S :

Growth yield from substrate S (g dry biomass [g substrate]−1)

References

  • Babel W (1982) Energetische und biochemische Aspekte der Mischsubstratfermentation. In: Ringpfeil M (Ed) Abhandlungen der Akademie der Wissenschaften der DDR (D2). ‘Biotechnologie’ (pp 183–188). Akademic Verlag, Berlin

    Google Scholar 

  • Bader FB (1982) Kinetics of double-substrate limited growth. In: Bazin MJ (Ed) Microbial Population Dynamics (pp 1–32). CRC Press, Boca Raton

    Google Scholar 

  • Baidya TKN, Webb FC & Lilly MD (1967) The utilization of mixed sugars in continuous fermentation. I. Biotechnol. Bioeng. 9: 195–204

    Google Scholar 

  • Baltzis BC & Fredrickson AG (1988) Limitation of growth rate by two complementary nutrients: some elementary but neglected considerations. Biotechnol. Bioeng. 31: 75–86

    Google Scholar 

  • Bazin MJ (Ed) (1982) Microbial Population Dynamics. CRC Series in Mathematical Models in Microbiology. CRC Press, Boca Raton

    Google Scholar 

  • Blanch H & Yoon H (1977) Competition for mixed substrates by microbial populations. Biotechnol. Bioeng. 19: 1193–1210

    PubMed  Google Scholar 

  • Busby SJW (1986) Positive regulation in gene expression. In: Booth IR & Higgins CF (Eds) Regulation of Gene Expression — 25 Years on (pp 51–77). University Press, Cambridge, UK

    Google Scholar 

  • Button DK (1985) Kinetics of nutrient-limited transport and microbial growth. Microbiol. Rev. 49: 270–297

    PubMed  Google Scholar 

  • Button DK (1993) Nutrient-limited microbial growth kinetics: Overview and recent advances. Antonie van Leeuwenhoek (this issue)

  • Egli T, Käppeli O & Fiechter A (1982) Mixed substrate growth of methylotrophic yeasts in chemostat culture: influence of the dilution rate on the utilisation of a mixture of glucose and methanol. Arch. Microbiol. 131: 8–13

    Google Scholar 

  • Egli T, Lindley ND & Quayle JR (1983) Regulation of enzyme synthesis and variation of residual methanol concentration during carbon-limited growth ofKloeckera sp. 2201 on mixtures of methanol and glucose. J. Gen. Microbiol. 129: 1269–1281

    Google Scholar 

  • Egli T & Mason CA (1991) Mixed substrates and mixed cultures. In: Goldberg I & Rokem JS (Eds) Biology of Methylotrophs (pp 173–201). Butterworth-Heinemann, Boston

    Google Scholar 

  • Gottschal JC (1993) Growth kinetics and competition — some contemporary comments. Antonie van Leeuwenhoek (this issue)

  • Harder W & Dijkhuizen L (1976) Mixed substrate utilization. In: Dean ACR, Ellwood DC, Evans CGT & Melling J (Eds) Continuous Culture, Vol 6: Applications and New Fields (pp 297–314). Ellis Harwood, Chichester

    Google Scholar 

  • Harder W & Dijkhuizen L (1982) Strategies of mixed substrate utilization. Philos. Trans. R. Soc. London Ser. B 297: 459–479

    Google Scholar 

  • Harte MJ & Webb FC (1967) Utilization of mixed sugars in continuous fermentation. II. Biotechnol. Bioeng. 9: 205–221

    Google Scholar 

  • Jannasch HW & Egli T (1993) Microbial growth kinetics: a historical perspective. Antonie van Leeuwenhoek (this issue)

  • Kompala ES, Ramakrishna D & Tsao GT (1984) Cybernetic modeling of microbial growth on multiple substrates. Biotechnol. Bioeng. 26: 1272–1281

    Google Scholar 

  • Law AT & Button DK (1977) Multiple-carbon-source-limited growth kinetics of a marine coryneform bacterium. J. Bacteriol. 129: 115–123

    PubMed  Google Scholar 

  • Lee AL, Ataai MM & Shuler ML (1984). Double substrate limited growth ofEscherichia coli. Biotechnol. Bioeng. 26: 1389–1401

    Google Scholar 

  • Lendenmann U, Snozzi M & Egli T (1992) Simultaneous utilization of diauxic sugar mixtures byEscherichia coli. 6th International Symposium on Microbial Ecology. Abstracts, p 254. Barcelona, Spain

  • Lengeler JW (1993) Carbohydrate transport in bacteria under environmental conditions, a black box? Antonie van Leeuwenhoek (this issue)

  • Magasanik B & Neidhardt FC (1987) Regulation of carbon and nitrogen utilization. In: Ingraham JL, Brooks Low K, Magasanik B, Schaechter M & Umbarger HE (Eds)Escherichia coli andSalmonella typhimurium (pp 1328–1325). American Society for Microbiology, Washington, DC

    Google Scholar 

  • Mankad T & Bungay HR (1988) Models for microbial growth with more than one limiting nutrient. J. Biotechnol. 7: 161–166

    Google Scholar 

  • Mateles RI, Chian SK & Silver R (1967) Continuous culture on mixed substrates. In: Powell PO, Evans CGT, Strange RE & Tempest DW (Eds) Microbial Physiology and Continuous Culture (pp 232–239). H.S.M.O., London

    Google Scholar 

  • Matin A (1979) Microbial regulatory mechanisms at low nutrient concentrations as studied in chemostat. In: Shilo M (Ed) Strategies of Microbial Life in Extreme Environments (pp 323–339). Dahlem Konferenzen, Berlin

    Google Scholar 

  • MeGee RD, Drake JF, Fredrickson AG & Tsuchiya HM (1972) Studies in intermicrobial symbiosis,Saccharomyces cerevisiae andLactobacillus casei. Can. J. Microbiol. 18: 1733–1742

    PubMed  Google Scholar 

  • Monod J (1942) Recherches sur la Croissance des Cultures Bactériennes. Hermann & Cie., Paris

    Google Scholar 

  • Münster U (1993) Concentrations and fluxes of organic carbon substrates in the aquatic environment. Antonie van Leeuwenhoek (this issue)

  • Münster U & Chróst RJ (1990) Origin, composition, and microbial utilization of dissolved organic matter. In: Overbeck J & Chróst RJ (Eds) Aquatic Microbial Ecology Biochemical and Molecular Approaches (pp 8–46). Springer, New York

    Google Scholar 

  • NG FM-W & Dawes EA (1973) Chemostat studies on the regulation of glucose metabolism inPseudomonas aeruginosa by citrate. Biochem. J. 132: 129–140

    PubMed  Google Scholar 

  • Postma PW (1986) Catabolite repression and related processes. In: Booth IR & Higgins CF (Eds) Regulation of Gene Expression — 25 Years on (pp 21–49). University Press, Cambridge, UK

    Google Scholar 

  • Powell EO (1967) The growth rate of micro-organisms as a function of substrate concentration. In: Powell EO, Evans CGT, Strange RE & Tempest DW (Eds) Microbial Physiology and Continuous Culture. Proceedings of the 3rd International Symposium on Continuous Culture of Microorganisms (pp 34–55). H.M.S.O., London

    Google Scholar 

  • Rutgers M, Balk TA & van Dam K (1990) Quantification of multiple-substrate controlled growth: simultaneous ammonium and glucose limitation in chemostat cultures ofKlebsiella pneumoniae. Arch. Microbiol. 153: 478–484

    PubMed  Google Scholar 

  • Rutgers M, van Dam K & Westerhoff HV (1991) Control and thermodynamics of microbial growth. Rational tools for bioengineering. CRC Crit. Rev. Biotechnol. 11: 367–395

    Google Scholar 

  • Senn H (1989) Kinetik und Regulation des Zuckerabbaus vonEscherichia coli ML30 bei tiefen Zuckerkonzentrationen. PhD Thesis ETH Nr. 8831, Zürich

  • Senn H, Lendenmann U, Snozzi M, Hamer G & Egli T (1993) The growth ofEscherichia coli in glucose-limited chemostat cultures: A reexamination of the kinetics. Biochim. Biophys. Acta (submitted)

  • Silver RS & Mateles RI (1969) Control of mixed-substrate utilization in continuous cultures ofEscherichia coli. J. Bacteriol. 97: 535–543

    PubMed  Google Scholar 

  • Simkins S & Alexander M (1984) Models for mineralization kinetics with the variables of substrate concentration and population density. Appl. Environ. Microbiol. 47: 1299–1306

    PubMed  Google Scholar 

  • Wanner U & Egli T (1990) Dynamics of microbial growth and cell composition in batch culture. FEMS Microbiol. Rev. 75: 19–44

    Google Scholar 

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Authors and Affiliations

  1. Swiss Federal Institute for Environmental Science and Technology (EAWAG) and Swiss Federal Institute of Technology (ETH), Überlandstrasse 133, CH-8600, Dübendorf, Switzerland

    Thomas Egli, Urs Lendenmann & Mario Snozzi

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  1. Thomas Egli
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  2. Urs Lendenmann
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  3. Mario Snozzi
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Egli, T., Lendenmann, U. & Snozzi, M. Kinetics of microbial growth with mixtures of carbon sources. Antonie van Leeuwenhoek 63, 289–298 (1993). https://doi.org/10.1007/BF00871224

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