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Front. Microbiol. | doi: 10.3389/fmicb.2018.01357

On the natural history of flavin-based electron bifurcation

Frauke Baymann1, Barbara Schoepp-Cothenet1, Simon Duval1,  Marianne Guiral1,  Myriam Brugna1,  Carole Baffert2, Michael J. Russell3 and  Wolfgang Nitschke1*
  • 1Bioénergétique et Ingénierie des Protéines (BIP) UMR7281, Centre National de la recherche Scientifique, Marseille, France
  • 2CNRS, BIP, UMR 7281, IMM FR3479, Aix-Marseille Université, France
  • 3Jet Propulsion Laboratory, California Institute of Technology, United States

Electron bifurcation is here described as a special case of the continuum of electron transfer reactions accessible to two-electron redox compounds with redox cooperativity. We argue that electron bifurcation is foremost an electrochemical phenomenon based on (a) strongly inverted redox potentials of the individual redox transitions, (b) a high endergonicity of the first redox transition and (c) an escapement-type mechanism rendering completion of the first electron transfer contingent on occurrence of the second one. This mechanism is proposed to govern both the traditional quinone-based and the newly discovered flavin-based versions of electron bifurcation. Conserved and variable aspects of the spatial arrangement of electron transfer partners in flavoenzymes are assayed by comparing the presently available 3D structures. A wide sample of flavoenzymes is analyzed with respect to conserved structural modules and three major structural groups are identified which serve as basic frames for the evolutionary construction of a plethora of flavin-containing redox enzymes. We argue that flavin-based and other types of electron bifurcation are of primordial importance to free energy conversion, the quintessential foundation of life, and discuss a plausible evolutionary ancestry of the mechanism.

Keywords: Electron bifurcation, Redox cooperativity, flavoenzymes, Emergence of life, redox enzyme construction kit, Bioenergetics

Received: 06 Apr 2018; Accepted: 05 Jun 2018.

Edited by:

Michael W. Adams, University of Georgia, United States

Reviewed by:

Wolfgang Buckel, Philipps University of Marburg, Germany
Pia Ädelroth, Stockholm University, Sweden  

Copyright: © 2018 Baymann, Schoepp-Cothenet, Duval, Guiral, Brugna, Baffert, Russell and Nitschke. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Wolfgang Nitschke, Centre National de la recherche Scientifique, Marseille, Bioénergétique et Ingénierie des Protéines (BIP) UMR7281, 31 chemin Joseph-Aiguier, CS 70071, Marseille, 13402, France, nitschke@imm.cnrs.fr