Phototrophic Gemmatimonadetes evolved the ability to use solar energy following horizontal transfer of photosynthesis-related genes from an ancient phototrophic proteobacterium. The electron cryo-microscopy structure of the Gemmatimonas phototrophica photosystem at 2.4 Å reveals a unique, double-ring complex. Two unique membrane-extrinsic polypeptides, RC-S and RC-U, hold the central type 2 reaction center (RC) within an inner 16-subunit light-harvesting 1 (LH1) ring, which is encircled by an outer 24-subunit antenna ring (LHh) that adds light-gathering capacity. Femtosecond kinetics reveal the flow of energy within the RC-dLH complex, from the outer LHh ring to LH1 and then to the RC. This structural and functional study shows that G. phototrophica has independently evolved its own compact, robust, and highly effective architecture for harvesting and trapping solar energy.

BioEM lab Biozentrum University of Basel Mattenstrasse 26 4058 Basel Switzerland

Cambridge Institute for Medical Research University of Cambridge Cambridge CB2 0XY UK

Center Algatech Institute of Microbiology Czech Academy of Sciences 37981 Třeboň Czechia

Department of Chemistry University of York York YO10 5DD UK

Department of Plant and Environmental Sciences University of Copenhagen Nørregade 10 DK 1165 Copenhagen Denmark

Electron Bio imaging Centre Diamond Light Source Didcot OX11 0DE UK

ELI Beamlines Institute of Physics of the Czech Academy of Sciences Na Slovance 1999 2 182 21 Prague Czechia

Faculty of Science University of South Bohemia 37005 České Budějovice Czechia

Lab of Molecular Structure Institute of Microbiology Czech Academy of Sciences Prague Czechia

Laboratory of Biological Electron Microscopy Institute of Physics SB EPFL and Faculty of Biology and Medicine Uni Lausanne CH 1015 Lausanne Switzerland

Materials and Structural Analysis Thermo Fisher Scientific Achtseweg Noord 5 5651 GG Eindhoven Netherlands

MRC Laboratory of Molecular Biology Francis Crick Avenue Cambridge CB2 0QH UK

School of Biosciences University of Sheffield Sheffield S10 2TN UK

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