Integrated Thermodynamic Analysis of Electron Bifurcating [FeFe]-Hydrogenase to Inform Anaerobic Metabolism and H2 Production

Katherine Chou, Pin-Ching Maness, Zackary Jay, Kristopher Hunt, Gerrit Schut, Michael Adams, Ross Carlson

Research output: Contribution to journalArticlepeer-review

14 Scopus Citations

Abstract

Electron bifurcating, [FeFe]-hydrogenases are recently described members of the hydrogenase family and catalyze a combination of exergonic and endergonic electron exchanges between three carriers (2 ferredoxinred + NAD(P)H + 3 H+ = 2 ferredoxinox + NAD(P)+ + 2 H2). A thermodynamic analysis of the bifurcating, [FeFe]-hydrogenase reaction, using electron path-independent variables, quantified potential biological roles of the reaction without requiring enzyme details. The bifurcating [FeFe]-hydrogenase reaction, like all bifurcating reactions, can be written as a sum of two non-bifurcating reactions. Therefore, the thermodynamic properties of the bifurcating reaction can never exceed the properties of the individual, non-bifurcating, reactions. The bifurcating [FeFe]-hydrogenase reaction has three competitive properties: 1) enabling NAD(P)H-driven proton reduction at pH2 higher than the concurrent operation of the two, non-bifurcating reactions, 2) oxidation of NAD(P)H and ferredoxin simultaneously in a 1:1 ratio, both are produced during typical glucose fermentations, and 3) enhanced energy conservation (~10 kJ mol−1 H2) relative to concurrent operation of the two, non-bifurcating reactions. Our analysis demonstrated ferredoxin E°′ largely determines the sensitivity of the bifurcating reaction to pH2, modulation of the reduced/oxidized electron carrier ratios contributed less to equilibria shifts. Hydrogenase thermodynamics data were integrated with typical and non-typical glycolysis pathways to evaluate achieving the ‘Thauer limit’ (4 H2 per glucose) as a function of temperature and pH2. For instance, the bifurcating [FeFe]-hydrogenase reaction permits the Thauer limit at 60 °C if pH 2 ≤ ~10 mbar. The results also predict Archaea, expressing a non-typical glycolysis pathway, would not benefit from a bifurcating [FeFe]-hydrogenase reaction; interestingly, no Archaea have been observed experimentally with a [FeFe]-hydrogenase enzyme.

Original languageAmerican English
Article number148087
Number of pages12
JournalBBA - Bioenergetics
Volume1861
Issue number1
DOIs
StatePublished - 2020

Bibliographical note

Publisher Copyright:
© 2019 Elsevier B.V.

NREL Publication Number

  • NREL/JA-2700-75647

Keywords

  • Bioenergetics
  • Electron bifurcation
  • Energy conservation
  • Molecular hydrogen
  • Thauer limit
  • Thermodynamics
  • [FeFe]-hydrogenase

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