Architecture and mechanism of the light-harvesting apparatus of purple bacteria

Abstract

Photosynthetic organisms fuel their metabolism with light energy and have developed for this purpose an efficient apparatus for harvesting sunlight. The atomic structure of the apparatus, as it evolved in purple bacteria, has been constructed through a combination of x-ray crystallography, electron microscopy, and modeling. The detailed structure and overall architecture reveals a hierarchical aggregate of pigments that utilizes, as shown through femtosecond spectroscopy and quantum physics, elegant and efficient mechanisms for primary light absorption and transfer of electronic excitation toward the photosynthetic reaction center.

Figure 1

Schematic representation of the photosynthetic apparatus in the intracytoplasmic membrane of purple bacteria. The RC (red) is surrounded by the light-harvesting complex I (LH-I, green) to form the LH-I–RC complex, which is surrounded by multiple light-harvesting complexes LH-II (green), forming altogether the PSU. Photons are absorbed by the light-harvesting complexes and excitation is transferred to the RC initiating a charge (electron-hole) separation. The RC binds quinone Q_B, reduces it to hydroquinone Q_BH₂, and releases the latter. Q_BH₂ is oxidized by the bc₁ complex, which uses the exothermic reaction to pump protons across the membrane; electrons are shuttled back to the RC by the cytochrome c₂ complex (blue) from the ubiquinone–cytochrome bc₁ complex (yellow). The electron transfer across the membrane produces a large proton gradient that drives the synthesis of ATP from ADP by the ATPase (orange). Electron flow is represented in blue, proton flow in red, and quinone flow, likely confined to the intramembrane space, in black.

Figure 2

Energy levels of the electronic excitations in the PSU of BChl a containing purple bacteria. The diagram illustrates a funneling of excitation energy toward the photosynthetic RC. The dashed lines indicate (vertical) intracomplex excitation transfer, and the solid lines (diagonal) indicate intercomplex excitation transfer. LH-I exists in all purple bacteria; LH-II exists in most species; LH-III arises in certain species only.

Figure 3

The octameric LH-II complex from Rs. molischianum (19). (a) The α-helical segments are represented as cylinders with the α-apoproteins (inside) in blue and the β-apoprotein (outside) in magenta. The BChl molecules are in green with phytyl tails truncated for clarity. The lycopenes are in yellow. (b) Arrangement of chromophores with BChls represented as squares, and with carotenoids (lycopenes) in a licorice representation. Bars connected with the BChls represent the Q_y transition dipole moments as defined by the vector connecting the N atom of pyrrol I and the N atom of pyrrol III (22). Representative distances between central Mg atoms of B800 BChl and B850 BChl are given in Å. The B850 BChls bound to the α-apoprotein and the β-apoprotein are denoted as B850a and B850b, respectively; BChl B850a′ is bound to the (left) neighboring heterodimer.

Figure 4

Structure of the LH-I–RC complex. (a) Side view of the LH-I–RC complex with three LH-I αβ-heterodimers on the front side removed to expose the RC in the interior. The α-helices are represented as cylinders with the L, M, and H subunits of the RC in yellow, red, and gray, and the α-apoprotein and the β-apoprotein of the LH-I in blue and magenta. BChls and bacteriopheophytins are represented as green and yellow squares, respectively. Carotenoids (spheroidenes) are in a yellow licorice representation, and quinone Q_B is rendered by gray van der Waals spheres. Q_B shuttles in and out (as Q_BH₂) of the LH-I–RC complex as indicated in Fig. 1. (b) Arrangement of BChls in the LH-I–RC complex. The BChls are represented as squares with B875 BChls of LH-I in green, and the special pair (P_A and P_B) and the accessory BChls (B_A and B_B) of the RC in red and blue, respectively; cyan bars represent Q_y transition moments of BChls. [Produced with the program vmd (25)].

Figure 5

Arrangement of pigment–protein complexes in the modeled bacterial PSU of Rb. sphaeroides. The α-helices are represented as C_α-tracing tubes with α-apoproteins of both LH-I and LH-II in blue and β-apoproteins in magenta, and the L, M, and H subunits of RC in yellow, red, and gray, respectively. All the BChls are in green, and carotenoids are in yellow. [Produced with the program vmd (25)].

Figure 6

BChl–carotenoid interactions. (Upper Left) Exciton bands of the circular B850 BChl aggregate as determined by quantum chemical (INDO/S) calculations (29) based on coordinates of the crystal structure of LH-II from Rs. molischianum (19). The degenerate states that carry all the oscillator strength are highlighted by thickened lines. (Upper Right) Excitation energies of BChl and carotenoid states in LH-II of Rb. sphaeroides. Solid lines represent spectroscopically measured energy levels. The dashed line indicates the estimated (see refs. and 47) energy for the optically forbidden S₁ state of the carotenoid spheroidene. (Lower) Arrangement of spheroidene and the most proximate BChls based on the modeled structure of LH-II from Rb. sphaeroides. Close contacts between BChl and the carotenoid spheroidene are indicated by representative distances (in angstroms).

Figure 7

Excitation transfer in the bacterial photosynthetic unit. LH-II contains two types of BChls, commonly referred to as B800 (dark blue) and B850 (green), which absorb at 800 nm and 850 nm, respectively. BChls in LH-I absorb at 875 nm and are labeled B875 (green). P_A and P_B refer to the RC special pair, and B_A, B_B refer to the accessory BChls in the RC. The figure demonstrates the coplanar arrangement of the B850 BChl ring in LH-II, the B875 BChl ring of LH-I, and the RC BChls P_A, P_B, B_A, B_B. [Produced with the program vmd (25)].

Figure 8

Schematic representation of proposed models of the PSUs in other photosynthetic systems. The figure displays inter- and extramembrane light-harvesting complexes, together with the RCs (RC in green bacteria, and PS-I and PS-II in cyanobacteria, dinoflagellates, and green plants). (a) Green bacteria: The major light-harvesting complex, chlorosome, contains rod-like BChl c aggregates surrounded by a layer of protein embedding lipids. Excitation energy harvested by the rod-like aggregates reaches the RC through a BChls a containing baseplate and membrane-bound light-harvesting BChl a complexes. (b) Cyanobacteria: The dominant light-harvesting complex of cyanobacteria and red algae, phycobilisome (PBS), is unique in choosing linear tetrapyrroles as pigments. Several types of disk-like pigment–protein complexes such as R-phycoerythrin (51) constitute the phycobilisome rods and core. (c) Dinoflagellates: The photosynthetic unit of dinoflagellates consists of several membrane-bound pigment–protein complexes and an extramembrane light-harvesting complex, the peridinin–chlorophyll–protein (PCP). (d) Green plants: Chloroplasts of green plants possess chlorophyll-carotenoid containing LHCII (6) as the most abundant light-harvesting complex. [Images of R-phycoerythrin and PCP were produced with the program vmd (25)].