Control of Photosystem Formation in Rhodobacter sphaeroides

Rhodobacter sphaeroides has the capacity to grow by aerobic and anaerobic respiration and photosynthetically in the light under anaerobic conditions, as well as fermentatively. It can fix atmospheric nitrogen and carbon dioxide. It resembles other gram-negative members of the class Proteobacteria when growing aerobically, but a reduction in oxygen tension induces an intracellular differentiation of the inner membrane, leading to the formation of the intracytoplasmic membrane system (ICM). The ICM houses the integral membrane pigment-protein complexes constituting the photosystem (PS), comprised of the reaction center (RC) and two light-harvesting (LH) complexes. For an early review of ICM biosynthesis, see reference 44. The LH complexes are designated B800-850 (LHII) and B875 (LHI), based on their respective absorption maxima. The ratio of LHI to RC is fixed at approximately 15:1, whereas the ratio of LHII to the LHI-RC unit is variable, changing in a manner inverse to the incident light intensity. These three pigment-protein complexes are the spectral complexes (SC) of the R. sphaeroides PS. Detailed structural information about these complexes in several species of Rhodobacter is emerging (72). The LH complexes capture light energy and direct that energy to the RC, where conversion of the excitation energy takes place and is intrinsically coupled with a cyclic flow of electrons, ultimately to the periplasmically localized cytochrome c2, which serves to rereduce the RC to allow a new cycle of electron flow (for further details, see references 42, 44, and 72). Bacteriochlorophyll (Bchl) absorbs most of the light energy within the SCs and is critical to the assembly and final structure of the SCs (44, 84, 87). The carotenoids (Crt) have a minor role in absorbing light energy (15), but they function to protect the complexes against photo-oxidative damage, dissipate excess radiant energy, and help to maintain the structure and relative abundance of each SC (35, 50, 53). A reduction in oxygen tension is both necessary and sufficient to induce synthesis of the ICM (reviewed in references 42 and 44), which is gratuitously produced under anaerobic dark growth conditions, in the presence of an alternate electron acceptor such as dimethyl sulfoxide (DMSO). Oxygen tension is the major environmental stimulus controlling PS induction, with variations in light intensity determining the cellular level of the ICM and the abundance of the different SCs. PS formation is tightly regulated, with checkpoints at all levels of information flow, from transcriptional through posttranslational. In the following sections, we will describe what we currently know about the regulatory processes controlling the formation and abundance of SCs in R. sphaeroides. We will present a working model for the regulation of PS formation in R. sphaeroides 2.4.1 which is based on the critical role of cellular redox carriers. For clarity, we will, throughout this review, define aerobic growth as that which occurs under highly oxygenic conditions, under which there are no detectable SCs present in wild-type membranes.