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Thermodynamics shapes the in vivo enzyme burden of glycolytic pathways

Journal Article · · mBio
 [1];  [2];  [2];  [3];  [3];  [1];  [2];  [1];  [4];  [3]
  1. Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
  2. Univ. of Wisconsin, Madison, WI (United States)
  3. Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
  4. Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States); Morgridge Institute for Research, Madison, WI (United States)

Thermodynamically constrained reactions and pathways are hypothesized to impose greater protein demands on cells, requiring higher enzyme amounts to sustain a given flux compared to those with stronger thermodynamics. To test this, we quantified the absolute concentrations of glycolytic enzymes in three bacterial species—Zymomonas mobilis, Escherichia coli, and Clostridium thermocellum—which employ distinct glycolytic pathways with varying thermodynamic driving forces. By integrating enzyme concentration data with corresponding in vivo metabolic fluxes and ΔG measurements, we found that the highly favorable Entner-Doudoroff pathway in Z. mobilis requires only one-fourth the amount of enzymatic protein to sustain the same flux as the thermodynamically constrained pyrophosphate-dependent glycolytic pathway in C. thermocellum, with the Embden-Meyerhof-Parnas pathway in E. coli exhibiting intermediate thermodynamic favorability and enzyme demand. Across all three pathways, early reactions with stronger thermodynamic driving forces generally required lower enzyme investment than later, less favorable steps. Additionally, reflecting differences in glycolytic strategies, the highly reversible ethanol fermentation pathway in C. thermocellum requires 10-fold more protein to maintain the same flux as the irreversible, forward-driven ethanol fermentation pathway in Z. mobilis. Thus, protein investment across glycolytic pathways reflects differences in their thermodynamic favorability.

Research Organization:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
Grant/Contract Number:
SC0018409; SC0018998
OSTI ID:
2588573
Journal Information:
mBio, Journal Name: mBio Journal Issue: 10 Vol. 16; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

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