Photosynthesis in the Purple Bacteria

Abstract

Anoxygenic chlorophototrophic purple bacteria have long provided a useful model system for functional and structural studies of the light reactions of photosynthesis, since they possess only a single Type II photochemical reaction center (RC), while in the more complex oxygenic phototrophs, two types of RCs, designated as photosystems I and II, are formed. The first of the major recent research breakthrough described here is the elucidation of the X-ray structure of the RC-light harvesting 1 (LH1) core complex of purple bacteria at near-atomic (3.0 A) resolution. This structure represents an important landmark in structural biology, since along with the available structures of the peripheral LH2 antenna and RC proteins, a complete structural basis for both primary excitation and electron transfer reactions has now emerged. Importantly, in the closed, elliptical ring-like LH1 structure, channels exist that are compatible with the passage of quinol molecules for exchange with the quinone/quinol pool. Another significant advance in understanding the structural basis for the photosynthetic primary reactions is represented by the elegant views of the supramolecular surface organization of native intracytoplasmic membranes (ICMs) obtained by atomic force microscopy (AFM). These topographs uncovered a wide diversity of species-dependent arrangements of closely packed LH2 and RC-LH1 complexes, which in Rhodobacter sphaeroides, consisted of a well-organized architecture, made up of ordered, interconnected RC-LH1 networks intercalated by rows of LH2, coexisting with LH2-only domains. A less regular organization, with mixed regions of LH2 and RC-LH1 cores, intermingled with large, paracrystalline domains, was observed in other peripheral antenna-containing species, notably Rhodospirillum photometricum and Rhodopseudomonas palustris. These several types of supramolecular organizations are all capable of fulfilling the basic requirements for efficient collection, transmission, and trapping of radiant energy. Recently, the cytochrome bc1 complex was also localized by AFM, using gold labelling in Rba. sphaeroides and found to be mainly confined to disordered areas adjacent to RC–LH1 core structures. Also described here are alterations in membrane dynamics and in excitation energy transfer capabilities that occur during adaptation of Rba. sphaeroides from high to low intensity illumination. These changes apparently arise from constraints on the flow of redox species on both the RC donor and acceptor sides, imposed by accumulation of large LH2 domains in the bilayer in which only a fraction of the LH2 rings are well connected to the RC. Advances in the proteomics of ICM development have also been made in which ICM growth initiation sites were found to be enriched in cytoplasmic membrane (CM) markers, including electron transfer proteins and permeases as well as general membrane protein assembly factors, confirming the origins of this membrane fraction from both peripheral respiratory membrane and sites of active CM invagination. Lastly, a computational and systems biology approach is discussed for determining the ATP production rate and energy conversion efficiency of a single chromatophore vesicle, based upon considerations from a quantitative supramolecular structural model.