Mechanisms of Energy Transduction by Charge Translocating Membrane Proteins

Abstract

Life relies on the constant exchange of different forms of energy, i.e., on energy transduction. Therefore, organisms have evolved in a way to be able to harvest the energy made available by external sources (such as light or chemical compounds) and convert these into biological useable energy forms, such as the transmembrane difference of electrochemical potential (Δμ). Membrane proteins contribute to the establishment of Δμb y coupling exergonic catalytic reactions to the translocation of charges (electrons/ions) across the membrane. Irrespectively of the energy source and consequent type of reaction, all charge-translocating proteins follow two molecular coupling mechanisms: direct-or indirectcoupling, depending on whether the translocated charge is involved in the driving reaction. In this review, we explore these two coupling mechanisms by thoroughly examining the different types of charge-translocating membrane proteins. For each protein, we analyze the respective reaction thermodynamics, electron transfer/catalytic processes, charge-translocating pathways, and ion/substrate stoichiometries.

The Ion-Translocating NrfD-Like Subunit of Energy-Transducing Membrane Complexes

“…Our identification is supported by substitution studies of amino acid residues located at TMH 1-4 on our proposed N-side half-channel (Tyr106 PsrC_W and Glu146 PsrC_W ) and located at TMH 5-8 on the P-side half-channel (Glu225 PsrC_W , Ser185 PsrC_W , Ser188 PsrC_W and Tyr310 PsrC_W ) of W. succinogenes PsrC model, resulted in strains with a compromised polysulfide respiration (Dietrich and Klimmek, 2002). These data suggest those residues may be important for proton translocation, since PsrABC catalyzes an endergonic reaction dependent of electrochemical potential (Dietrich and Klimmek, 2002;Calisto et al, 2021).…”

“…NrfD-like subunit-containing complexes were hypothesized to be capable of ion-translocation across the membrane (Calisto et al, 2021) and, in fact, proton-conducting pathways have been identified in the structures of the PsrC, ActC and ActF subunits (Jormakka et al, 2008;Sousa et al, 2018;Sun et al, 2018;Shi et al, 2020). Proton-conducting pathways are formed by amino acid residues with side chains that can establish hydrogen bonds, constituting a hydrogen bond network.…”

“…Our structural models reinforce the possible existence of ion-translocation pathways in all NrfD-like subunits and the contribution of the NrfD-like subunit-containing complexes to energy transduction. NrfD-like subunit-containing complexes may perform energy transduction by an indirect-coupling mechanism and may generate or consume electrochemical potential (Calisto et al, 2021). W. succinogenes PsrABC activity was shown to be dependent on electrochemical potential (Dietrich and Klimmek, 2002), while QrcABCD activity was shown to be coupled to the formation of electrochemical potential (Duarte et al, 2018).…”

“…Energy transducing membrane complexes are usually composed of catalytic subunits and transmembrane proteins that perform translocation of charges, electrons or cations, across the membrane (Calisto et al, 2021). The most common membrane charge-translocating subunits so far observed in energy transduction complexes are the di-heme cytochrome b-like subunits and the so called NrfD-like subunits.…”

“…ActF does not contain any quinone/quinol binding site and it is the only NrfD-like subunit present in a complex in which another subunit of this type (which contains a quinone/quinol-binding site) is present. In addition, for all these subunits, putative ion-conducting pathways were proposed (Calisto et al, 2021). NrfD-like proteins also function as the link of the peripheral subunits to the membrane (Figure 1).…”