Remodeling of light-harvesting protein complexes in Chlamydomonas in response to environmental changes

Photosynthesis is dependent on light. Photosynthetic organisms struggle their entire lives to optimize photosynthetic function and minimize photooxidative damage in response to light quantity and quality. When the absorbed light energy exceeds the capacity of photosynthetic energy consumption, overreduction of electron transport carriers and accumulation of excitation energy in the light-harvesting-antennae may occur. The latter favors the production of excited triplet-state chlorophyll molecules ((3)Chl) that can interact with O-2, to cause the formation of reactive singlet oxygen (O-1(2),). The former favors the direct reduction of 0, by photosystem I (PSI) and the subsequent generation of reactive oxygen species, such as superoxide (O-2(-)), hydrogen peroxide (H2O2), and the hydroxyl radical (OH) (5, 6, 75). These reactive oxygen species are able to cause photo-oxidative damage to photosystem II (PSII), a primary target for photoinhibition (2, 4, 9), but also to PSI (59, 60), in particular under weak light at chilled temperatures (111, 121). Thus, adaptation mechanisms that balance the energy input, through photochemistry via the photosynthetic machinery, with the energy output through CO, assimilation and other metabolic pathways, are essential for plant survival. The function of the light-harvesting complexes (LHCs) is, as the name implies, to increase the effective absorption cross-section of the photosystems and to supply them with excitation energy. The LHCs bind chlorophyll a and b but lack any photochemical activity of their own. Both PSI and PSII have their own core antenna pigments, but the addition of the LHCs increases the number of antenna pigments connected to each reaction center by a factor of 2 to 4, depending upon the conditions (47). Energy transfer operates in a time scale of femtoseconds to picoseconds. The transfer time of excitation energy between neighboring Chl molecules in the antenna has been estimated to be 100 to 300 fs (45). It had long been known that the pigment molecules must be closely packed to allow such fast and efficient transfer, a supposition beautifully confirmed by the emergence of the X-ray crystal structures of PSI (65), PSII (42, 66, 135), and LHCI-PSI (12) in the last several years (see discussion below). On average, excitation energy makes 100 to 1,000 such hops between antenna chlorophylls before it is trapped at a reaction center. Depending upon the arrangement of pigment molecules within LHCs and of LHCs vis-a-vis the photosystems, excitation energy can be directed to specific photosystems, temporarily trapped on low-energy chlorophylls, or even converted to heat by nonphotochemical quenching. It does not require a great stretch of imagination to see how evolution might have taken advantage of such possibilities for the development of regulatory mechanisms to deal with variable illumination. The regulation of light energy input and distribution, by the dynamic regulation of the light-harvesting system, probably plays the most important role in balancing the light and dark reactions of photosynthesis. Light-harvesting systems and their functioning in algae and vascular plants have been addressed and discussed in numerous reviews (47, 58, 69, 101). Over the last decade the eukaryotic unicellular green alga Chlamydomonas reinhardtii has emerged as a potent model system for studying assembly, function, and regulation of the photosynthetic machinery in general (48, 51, 57, 98). Chlamydomonas has proven to be an excellent genetic model system for investigating different features of the regulation of light energy input and distribution, such as the role of the violaxanthin cycle in protection from photo-oxidative stress (89, 90) or the function of a specific PSII-associated major light-harvesting protein in nonradiative dissipation of excess excitation energy under high-light conditions (39) and other aspects that are addressed in more detail below. Further strengths of this model system evolve from an ongoing genomic project (>180,000 expressed sequence tag [EST] sequences have been obtained, and the second version of >9-fold whole-genome shotgun coverage was recently released by the U.S. Department of Energy Joint Genome Institute in February 2004), powerful genetics, and molecular techniques, as well as applicability to in-depth biochemical and structural analyses. In this review it is our aim to discuss recent developments in elucidating the composition, structural features, and dynamics of light-harvesting proteins in response to environment changes in C. reinhardtii.