A cytochrome c551 mediates the cyclic electron transport chain of the anoxygenic phototrophic bacterium Roseiflexus castenholzii
Lu Yu, Zhenzhen Min, Menghua Liu, Yueyong Xin, Aokun Liu, Jian Kuang, Wenping Wu, Jingyi Wu, Huimin He, Jiyu Xin, Robert E. Blankenship, Changlin Tian, Xiaoling Xu
Abstract
Roseiflexus castenholzii is a gram-negative filamentous phototrophic bacterium that carries out anoxygenic photosynthesis through a cyclic electron transport chain (ETC). The ETC is composed of a reaction center (RC)-light harvesting (LH) complex (rcRC-LH), an alternative complex III (rcACIII), which functionally replaces the cytochrome bc1/b6f complex, and the periplasmic electron acceptor auracyanin (rcAc). Although compositionally and structurally different from the bc1/b6f complex, rcACIII plays similar essential roles in oxidizing menaquinol and transferring electrons to the rcAc. However, rcACIII-mediated electron transfer (which includes both an intra-protein route and a downstream route) has not been clearly elucidated, nor have the details of cyclic ETC. Herein, we identified a previously unknown monoheme cytochrome c (cyt c551) as a novel periplasmic electron acceptor of rcACIII, it reduced the light-excited rcRC-LH to complete a cyclic ETC. We also revealed the molecular mechanisms involved in ETC using electron paramagnetic resonance (EPR), spectroelectrochemistry, enzymatic and structural analyses. We found that electrons released from rcACIII-oxidized menaquinol were transferred to two alternative periplasmic electron acceptors (rcAc and cyt c551), which eventually reduced the rcRC to form the complete cyclic ETC. This work serves as a foundation for further studies of ACIII-mediated electron transfer in anoxygenic photosynthesis, and broadens the understanding of the diversity and molecular evolution of the prokaryotic ETCs.