Cryo-EM structures of light-harvesting 2 complexes from Rhodopseudomonas palustris reveal the molecular origin of absorption tuning

• Published in: Proceedings of the National Academy of Sciences - PNAS 2022-10, Vol.119 (43), p.1-e2210109119
• Main Authors: Qian, Pu, Nguyen-Phan, Cam T., Gardiner, Alastair T., Croll, Tristan I., Roszak, Aleksander W., Southall, June, Jackson, Philip J., Vasilev, Cvetelin, Castro-Hartmann, Pablo, Sader, Kasim, Hunter, C. Neil, Cogdell, Richard J.
• Format: Article
• Language: English
• Subjects: Absorption; Absorption spectra; Antennas; BASIC BIOLOGICAL SCIENCES; Biological Sciences; Complexity; Deletion mutant; Electron microscopy; Genomes; Hydrogen bonding; Hydrogen bonds; Photosynthesis; Polypeptides; PucBA gene; Rhodopseudomonas palustris; Tuning
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2210109119

The genomes of some purple photosynthetic bacteria contain a multigene puc family encoding a series of α- and β-polypeptides that together form a heterogeneous antenna of light-harvesting 2 (LH2) complexes. To unravel this complexity, we generated four sets of puc deletion mutants in Rhodopseudomonas palustris , each encoding a single type of pucBA gene pair and enabling the purification of complexes designated as PucA-LH2, PucB-LH2, PucD-LH2, and PucE-LH2. The structures of all four purified LH2 complexes were determined by cryogenic electron microscopy (cryo-EM) at resolutions ranging from 2.7 to 3.6 Å. Uniquely, each of these complexes contains a hitherto unknown polypeptide, γ, that forms an extended undulating ribbon that lies in the plane of the membrane and that encloses six of the nine LH2 αβ-subunits. The γ-subunit, which is located near to the cytoplasmic side of the complex, breaks the C9 symmetry of the LH2 complex and binds six extra bacteriochlorophylls (BChls) that enhance the 800-nm absorption of each complex. The structures show that all four complexes have two complete rings of BChls, conferring absorption bands centered at 800 and 850 nm on the PucA-LH2, PucB-LH2, and PucE-LH2 complexes, but, unusually, the PucD-LH2 antenna has only a single strong near-infared (NIR) absorption peak at 803 nm. Comparison of the cryo-EM structures of these LH2 complexes reveals altered patterns of hydrogen bonds between LH2 αβ-side chains and the bacteriochlorin rings, further emphasizing the major role that H bonds play in spectral tuning of bacterial antenna complexes.