Structural Basis of Light Harvesting by Carotenoids: Peridinin-Chlorophyll-Protein from Amphidinium carterae

Abstract

Peridinin-chlorophyll-protein, a water-soluble light-harvesting complex that has a bluegreen absorbing carotenoid as its main pigment, is present in most photosynthetic dinoflagellates. Its high-resolution (2.0 angstrom) x-ray structure reveals a noncrystallographic trimer in which each polypeptide contains an unusual jellyroll fold of the a-helical amino-and carboxyl-terminal domains. These domains constitute a scaffold with pseudo-twofold symmetry surrounding a hydrophobic cavity filled by two lipid, eight peridinin, and two chlorophyll a molecules. The structural basis for efficient excitonic energy transfer from peridinin to chlorophyll is found in the clustering of peridinins around the chlorophylls at van der Waals distances. Table 1. Crystallographic data. Data collection: Native1 and derivative data (5 IllM K 2 PtCI 4 , 1-day soak) were collected on a rotating anode source (CuKa, 40 kV, 100 mA) with a STOE (Darmstadt, Germany) imaging plate detector. Native2 was collected at the BW7B wiggler bealllline at DESY on a 30-cm MARresearch (Hamburg, Germany) image plate. All data were processed with XDS (26). Phasing: Six heavy-atom binding sites were found using SHELXS (27) in Patterson search mode, and four additional sites were found by inspection of difference Fourier maps. Refinement of heavy-atom parameters was done with DAREFI (28). The phases could be improved further by inclusion of the anomalous signal and the use of solvent flattening and noncrystallographic symmetry averaging of the trimer in the asymmetric unit (29). Model building and refinement: The resulting 2.9 Aelectron density map was readily interpret-able. An initial model of PCP was built with 0 (23). The full sequence could be included, and 10 pigments were modeled. The initial model was refined with X-PLOR (24), including simulated annealing, positional refinement, and manual rebuilding against Native1 and later Native2. Strong noncrystallographic symmetry restraints were applied throughout the refinement. ARP (30) was used to obtain unbiased atomic positions for well-connected density in the 2.0 Adifference electron-density map. The arrangement of these atoms, together with possible hydrogen-bonding patterns, was consistent with an interpretation as DGDG molecules. After refinement, the DGDG head groups obey good stereochemistry and show no difference density. tuolecules. Within each cluster, the efficiency of singlet energy transfer fr01n peridinin to chlorophyll is close to unity (7). Models of chromophore interaction within and atuong the clusters have previously been based on spectroscopic investigations (7,8). Structural infornlation, such as that available for 1uenl-brane-bound LHCs fron1 higher plants (3) and bacteria (9), has greatly enhanced our understanding of antenna systen1s having chlorophyll as the n1ain pignlent. The highresolution structure of PCP gives insight into the highly organized structural basis of lightharvesting by carotenoids and its efficient transfer to chlorophyll and should be of considerable value for re...

Importance and Nature of Short-Range Excitonic Interactions in Light Harvesting Complexes and Organic Semiconductors

“…23,40,42,51 We include PCP in our study as a representative LHC containing two different type of chromophores: two pseudo-twofold symmetric sets of peridinin chromophores (carotenoids) and a pair of chlorophyll-a (ChlA) chromophores. 48,52 The arrangement of chromophores in these structures is illustrated in Figure 1.…”

“…48 The FMO protein has become the model system for much research into exciton transport in LHCs since the initial report of coherent energy transfer. 41,49 Comprising of three identical subunits containing 8 bacteriochlorophyll-a (BChlA) chromophores each, FMO is relatively simple from a chemical perspective, but is topologically complex, with no symmetry to the spatial arrangement of chromophores in space within a monomeric unit.…”

Metal-Enhanced Fluorescence of Chlorophylls in Single Light-Harvesting Complexes

“…Organized in two clusters, it contains two Chl a (green) and eight peridinin (Pers, orange) pigments that are closely packed within the hydrophobic cavity formed by the protein and a lipid (blue). 26 The distance between the two Chls a is 17.4 Å. The absorption spectrum (Figure 1b) shows that PCP utilizes the carotenoid, Per, as its primary pigment, which is responsible for the dominant absorption band in the blue-green spectral region (350 to 550 nm).…”

Circadian Changes in Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Distribution Inside Individual Chloroplasts Can Account for the Rhythm in Dinoflagellate Carbon Fixation

“…Although the control mechanism of this rhythm is not understood, it is possible that it may involve the soluble light-harvesting peridininchlorophyll a -protein (PCP), because this protein feeds energy primarily into photosystem II (Govindjee et al, 1979). Curiously, dinoflagellates are the only organisms known to use PCP in light harvesting, and the structure of this soluble protein is unlike that of any other light-harvesting protein (Norris and Miller, 1994;Hofmann et al, 1996).In addition to the unusual light-harvesting protein PCP, dinoflagellates also are the only known organisms whose chloroplasts contain a form II ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) (Morse et al, 1995;Rowan et al, 1996). The form II enzyme is composed of only large subunits and shares limited sequence identity with the form I enzyme (Narang et al, 1984).…”