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Role of phosphate in the central metabolism of two lactic acid bacteria – a comparative systems biology approach

Authors

  • Jennifer Levering,

    1.  Department of Modeling of Biological Processes, COS Heidelberg/BIOQUANT, University of Heidelberg, Germany
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    • These authors contributed equally to this work

  • Mark W. J. M. Musters,

    1.  Laboratory of Microbiology, Wageningen University, The Netherlands
    2.  Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
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    • These authors contributed equally to this work

  • Martijn Bekker,

    1.  Laboratory for Microbiology, Swammerdam Institute for Life Sciences, Amsterdam, The Netherlands
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    • These authors contributed equally to this work

  • Domenico Bellomo,

    1.  Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2.  Systems Bioinformatics IBIVU/Netherlands Consortium for Systems Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, The Netherlands
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  • Tomas Fiedler,

    1.  Institute of Medical Microbiology, Virology and Hygiene, Rostock, Germany
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  • Willem M. de Vos,

    1.  Laboratory of Microbiology, Wageningen University, The Netherlands
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  • Jeroen Hugenholtz,

    1.  Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2.  Laboratory for Microbiology, Swammerdam Institute for Life Sciences, Amsterdam, The Netherlands
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  • Bernd Kreikemeyer,

    1.  Institute of Medical Microbiology, Virology and Hygiene, Rostock, Germany
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  • Ursula Kummer,

    1.  Department of Modeling of Biological Processes, COS Heidelberg/BIOQUANT, University of Heidelberg, Germany
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  • Bas Teusink

    1.  Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2.  Systems Bioinformatics IBIVU/Netherlands Consortium for Systems Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, The Netherlands
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B. Teusink, Systems Bioinformatics IBIVU/Netherlands Consortium for Systems Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands
Fax: +31(0)205989435
Tel: + 31(0)205989435
E-mail: b.teusink@vu.nl

Abstract

Lactic acid-producing bacteria survive in distinct environments, but show common metabolic characteristics. Here we studied the dynamic interactions of the central metabolism in Lactococcus lactis, extensively used as a starter culture in the dairy industry, and Streptococcus pyogenes, a human pathogen. Glucose-pulse experiments and enzymatic measurements were performed to parameterize kinetic models of glycolysis. Significant improvements were made to existing kinetic models for L. lactis, which subsequently accelerated the development of the first kinetic model of S. pyogenes glycolysis. The models revealed an important role for extracellular phosphate in the regulation of central metabolism and the efficient use of glucose. Thus, phosphate, which is rarely taken into account as an independent species in models of central metabolism, should be considered more thoroughly in the analysis of metabolic systems in the future. Insufficient phosphate supply can lead to a strong inhibition of glycolysis at high glucose concentrations in both species, but this was more severe in S. pyogenes. S. pyogenes is more efficient at converting glucose to ATP, showing a higher tendency towards heterofermentative energy metabolism than L. lactis. Our comparative systems biology approach revealed that the glycolysis of L. lactis and S. pyogenes have similar characteristics, but are adapted to their individual natural habitats with respect to phosphate regulation.

Database

The mathematical models described here have been submitted to the Online Cellular Systems Modelling Database and can be accessed at http://jjj.biochem.sun.ac.za/database/Levering/index.html free of charge.

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