Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii
( In collaboration with Prof. Xiaoling Xu from Huangzhou Normal University )
Figure 1. The cyclic electron transfer chain in Roseiflexus castenholzii.
Figure 2. The structure and electron transfer mechanism of ACIII in Roseiflexus castenholzii.
Figure 3. Proposed redox-coupled proton translocation mechanism of the photosynthetic ACIII.
Alternative complex III (ACIII) is a multi-subunit quinol:electron acceptor oxidoreductase found in both the respiratory and photosynthetic electron transport chains of bacteria. As a functional counterpart of the cyt bc1 complex, ACIII is involved in coupling quinol oxidation with transmembrane proton translocation. The coupling mechanism, however, is poorly understood. Here, we report the cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic ACIII from the photosynthetic bacterium Roseiflexus castenholzii at 3.3 ？ and 3.5 ？ resolutions, respectively, and propose a previously unrecognized redox-coupled proton translocation mechanism. We identified a menaquinol binding pocket at the periplasmic side and an adjacent [3Fe-4S] cluster that likely accepts released electrons upon menaquinol oxidation. An electron transfer wire comprising six hemes and four iron-sulfur clusters was capable of transferring electrons to periplasmic acceptors. We detected a proton translocation passage in which three strictly conserved, mid-passage residues are likely essential for coupling the redox-driven proton translocation across the membrane. The results of this study allow us to propose a coupling mechanism that links the respiratory and photosynthetic functions of the ACIII. This mechanism provides both a structural basis and conceptual insights for further investigations about the electron transfer and energy transformations underlying bacterial photophosphorylation.
Reference:
Shi Y.#, Xin Y.#, Wang C.#, Blankenship R.E., Sun F.* and Xu XL.* (2020) Cryo-EM structure of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii. Science Advances, 6 (31): eaba2739. doi: 10.1126/sciadv.aba2739.
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