Structural basis for energy transduction by respiratory alternative complex III

Abstract

Electron transfer in respiratory chains generates the electrochemical potential that serves as energy source for the cell. Prokaryotes can use a wide range of electron donors and acceptors and may have alternative complexes performing the same catalytic reactions as the mitochondrial complexes. This is the case for the alternative complex III (ACIII), a quinol:cytochrome c/HiPIP oxidoreductase. In order to understand the catalytic mechanism of this respiratory enzyme, we determined the structure of ACIII from Rhodothermus marinus at 3.9 Å resolution by single-particle cryo-electron microscopy. ACIII presents a so-far unique structure, for which we establish the arrangement of the cofactors (four iron–sulfur clusters and six c-type hemes) and propose the location of the quinol-binding site and the presence of two putative proton pathways in the membrane. Altogether, this structure provides insights into a mechanism for energy transduction and introduces ACIII as a redox-driven proton pump.

FAD/NADH Dependent Oxidoreductases: From Different Amino Acid Sequences to Similar Protein Shapes for Playing an Ancient Function

“…Considering (a) the role played by NDH-2/NDI-like proteins in bacterial/fungal respiration [7,25], (b) the direct interaction between a T. paradoxus flavoprotein oxidoreductase and a CytC-like protein [44], and (c) the recently proposed rotenone sensitive NADH:UQ oxidoreductase activity of AIF [11,12], it could be speculated that a direct interaction between AIF and CytC and other mitochondrial copper-binding proteins of the inner membrane [59][60][61] might also exist in Metazoan mitochondria, with several implications regarding AIF participation in mitochondrial respiration. These data are coherent with previous observations about alternative respiratory protein complexes [62][63][64][65].…”

Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii

“…S6B) in the actE gene sequence may be excised from the transcript or degraded following translation in cells or at some point before the final complex assembly. This phenomenon was also observed in the respiratory ACIII (17).…”

“…To elucidate the proposed conformational changes that were involved in the redox-driven proton translocation of respiratory ACIII (17), the vitrified air-oxidized and dithionite-reduced ACIII were individually subjected to cryo-EM single-particle analysis. A dataset of 257,815 particles of the air-oxidized ACIII was used to reconstruct an electron potential map with an average resolution of 3.3 Å and a local resolution extending to 2.5 Å ( fig.…”

Sulfite oxidation by the quinone-reducing molybdenum sulfite dehydrogenase SoeABC from the bacterium Aquifex aeolicus

“…The NrfD/PsrC/QrcD protein family is quite diverse and a different mechanism may be used by different enzymes of the family [63]. A third possibility cannot be at present discarded, in which SoeABC would be a true proton pump (as complex I) and protons would be translocated by SoeC from the cytoplasm to the periplasmic compartment ( Figure 5 and Figure A7 proposition 3) [54,62,63]. In this case, the reaction of the enzyme could be electrogenic and contribute to the pmf.…”