Binding proteins enhance specific uptake rate by increasing the substrate-transporter encounter rate.

E. Bosdriesz, S. Magnúsdóttir, F.J. Bruggeman, B. Teusink, D. Molenaar

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. Several advantages of using binding proteins in such uptake systems have been proposed. However, a systematic, rigorous and quantitative analysis of the function of binding proteins is lacking. By combining knowledge of selection pressure and physiochemical constraints, we derive kinetic, thermodynamic, and stoichiometric properties of binding-protein dependent transport systems that enable a maximal import activity per amount of transporter. Under the hypothesis that this maximal specific activity of the transport complex is the selection objective, binding protein concentrations should exceed the concentration of both the scarce nutrient and the transporter. This increases the encounter rate of transporter with loaded binding protein at low substrate concentrations, thereby enhancing the affinity and specific uptake rate. These predictions are experimentally testable, and a number of observations confirm them. Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. We combine knowledge of selection pressure and physiochemical constraints with mathematical modeling to elucidate the benefit these binding proteins confer. We show that, when the binding protein concentration exceeds both the nutrient and the transporter concentrations, they increase the substrate-transporter encounter rate and thereby the nutrient uptake rate.
Original languageEnglish
Article number12
Pages (from-to)2394-2407
JournalThe FEBS Journal
Issue number282
DOIs
Publication statusPublished - 2015

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Carrier Proteins
Substrates
Nutrients
Food
Active Biological Transport
Microorganisms
Pressure
Protein Transport
Thermodynamics
Kinetics
Chemical analysis

Cite this

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title = "Binding proteins enhance specific uptake rate by increasing the substrate-transporter encounter rate.",
abstract = "Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. Several advantages of using binding proteins in such uptake systems have been proposed. However, a systematic, rigorous and quantitative analysis of the function of binding proteins is lacking. By combining knowledge of selection pressure and physiochemical constraints, we derive kinetic, thermodynamic, and stoichiometric properties of binding-protein dependent transport systems that enable a maximal import activity per amount of transporter. Under the hypothesis that this maximal specific activity of the transport complex is the selection objective, binding protein concentrations should exceed the concentration of both the scarce nutrient and the transporter. This increases the encounter rate of transporter with loaded binding protein at low substrate concentrations, thereby enhancing the affinity and specific uptake rate. These predictions are experimentally testable, and a number of observations confirm them. Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. We combine knowledge of selection pressure and physiochemical constraints with mathematical modeling to elucidate the benefit these binding proteins confer. We show that, when the binding protein concentration exceeds both the nutrient and the transporter concentrations, they increase the substrate-transporter encounter rate and thereby the nutrient uptake rate.",
author = "E. Bosdriesz and S. Magn{\'u}sd{\'o}ttir and F.J. Bruggeman and B. Teusink and D. Molenaar",
year = "2015",
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language = "English",
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journal = "The FEBS Journal",
issn = "1742-464X",
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Binding proteins enhance specific uptake rate by increasing the substrate-transporter encounter rate. / Bosdriesz, E.; Magnúsdóttir, S.; Bruggeman, F.J.; Teusink, B.; Molenaar, D.

In: The FEBS Journal, No. 282, 12, 2015, p. 2394-2407.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Binding proteins enhance specific uptake rate by increasing the substrate-transporter encounter rate.

AU - Bosdriesz, E.

AU - Magnúsdóttir, S.

AU - Bruggeman, F.J.

AU - Teusink, B.

AU - Molenaar, D.

PY - 2015

Y1 - 2015

N2 - Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. Several advantages of using binding proteins in such uptake systems have been proposed. However, a systematic, rigorous and quantitative analysis of the function of binding proteins is lacking. By combining knowledge of selection pressure and physiochemical constraints, we derive kinetic, thermodynamic, and stoichiometric properties of binding-protein dependent transport systems that enable a maximal import activity per amount of transporter. Under the hypothesis that this maximal specific activity of the transport complex is the selection objective, binding protein concentrations should exceed the concentration of both the scarce nutrient and the transporter. This increases the encounter rate of transporter with loaded binding protein at low substrate concentrations, thereby enhancing the affinity and specific uptake rate. These predictions are experimentally testable, and a number of observations confirm them. Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. We combine knowledge of selection pressure and physiochemical constraints with mathematical modeling to elucidate the benefit these binding proteins confer. We show that, when the binding protein concentration exceeds both the nutrient and the transporter concentrations, they increase the substrate-transporter encounter rate and thereby the nutrient uptake rate.

AB - Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. Several advantages of using binding proteins in such uptake systems have been proposed. However, a systematic, rigorous and quantitative analysis of the function of binding proteins is lacking. By combining knowledge of selection pressure and physiochemical constraints, we derive kinetic, thermodynamic, and stoichiometric properties of binding-protein dependent transport systems that enable a maximal import activity per amount of transporter. Under the hypothesis that this maximal specific activity of the transport complex is the selection objective, binding protein concentrations should exceed the concentration of both the scarce nutrient and the transporter. This increases the encounter rate of transporter with loaded binding protein at low substrate concentrations, thereby enhancing the affinity and specific uptake rate. These predictions are experimentally testable, and a number of observations confirm them. Microorganisms rely on binding-protein assisted, active transport systems to scavenge for scarce nutrients. We combine knowledge of selection pressure and physiochemical constraints with mathematical modeling to elucidate the benefit these binding proteins confer. We show that, when the binding protein concentration exceeds both the nutrient and the transporter concentrations, they increase the substrate-transporter encounter rate and thereby the nutrient uptake rate.

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JO - The FEBS Journal

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SN - 1742-464X

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