Computational determination of the pigment binding motif in the chlorosome protein a of green sulfur bacteria

Abstract

We present a molecular-scale model of Bacteriochlorophyll a (BChl a) binding to the chlorosome protein A (CsmA) of Chlorobaculum tepidum, and the aggregated pigment–protein dimer, as determined from protein–ligand docking and quantum chemistry calculations. Our calculations provide strong evidence that the BChl a molecule is coordinated to the His25 residue of CsmA, with the magnesium center of the bacteriochlorin ring situated\3 A° from the imidazole nitrogen atom of the histidine sidechain, and the phytyl tail aligned along the nonpolar residues of the a-helix of CsmA. We also confirm that the Qy band in the absorption spectra of BChl a experiences a large (?16 to ?43 nm) redshift when aggregated with another BChl a molecule in the CsmA dimer, compared to the BChl a in solvent; this redshift has been previously established by experimental researchers. We propose that our model of the BChl a–CsmA binding motif, where the dimer contains parallel aligned N-terminal regions, serves as the smallest repeating unit in a larger model of the para-crystalline chlorosome baseplate protein.

Alternative Excitonic Structure in the Baseplate (BChl a–CsmA Complex) of the Chlorosome from Chlorobaculum tepidum

“…The baseplate structure seems to be less complex than proposed in ref . Our data support an arrangement of weakly coupled dimers, as reported in refs , , and , and exciton hopping along the 2D network of CsmA dimers to the low-energy trap at 818.3 nm, which emits at 825.7 nm. Thus, our data are consistent with the model reported in ref that baseplate CsmA proteins arranged as a 2D paracrystalline lattice bind one BChl a per CsmA protein, while EET can be understood in terms of a random walk on an energetically disordered network, where the excitation can move coherently within the DOS distribution of site energies. , Thus, an electronic excitation could visit many sites via hopping (i.e., downhill jumps) and “freeze” at the energetically broad low-energy trap that is most likely located at the interface between the baseplate and FMO proteins.…”

“…This in turn suggests that energy harvested by baseplate pigments can be efficiently transferred to FMO within the 2D lattice. The low-energy trap in the baseplate at 818.3 nm is most likely formed via exciton hopping, and HB data are consistent with dimers of CsmA proteins containing two BChl a molecules sandwiched between the hydrophobic regions and bound near the histidine. , In summary, our results indicate the following: (i) nonresonant and resonant HB spectra obtained at 5 K for the pure chlorosome–baseplate system question the recent suggestion that at least four BChl a are in close contact within the baseplate protein; (ii) there is a large static diagonal disorder of baseplate BChl a (absorption bandwidth ≈ 625 cm –1 ) with a localized trap state at 818.3 nm (fwhm ≈ 240 cm –1 ) that leads to emission at 825.7 nm; and (iii) the four excitonic states identified at 77 K via 2DES most likely correspond to contamination of the baseplate with the FMO antenna and possibly the RC. Finally, HB spectra show that EET from the chlorosome BChl c → BChl a of the baseplate and BChl a → BChl a (within the baseplate) occur in 2.9 ± 0.1 and 2.0 ± 0.1 ps, respectively, indicating that the baseplate receives the exciton quickly, rapidly directing it to the lowest-energy baseplate trap (with a maximum at 818.3 nm), which releases the exciton to the FMO complexes.…”

“…Stoichiometric measurements strongly indicate that in Chlorobaculum ( Cb. ) tepidum , one CsmA protein binds a single BChl a molecule, , and the presence of a single histidine residue (His25) supports this conclusion. , A detailed structure of the baseplate is not known, although several models of the BChl a –CsmA dimer have been proposed. − Interestingly, while the BChl dipole–dipole angles (30–125°) and center-to-center distances (7–18 Å) vary significantly in these models, the calculated dipole couplings (assuming |μ| = 6.1 D) are in the range of 30–35 cm –1 . Further studies of photosystems of various complexities (i.e., chlorosome–baseplate, chlorosome–baseplate–FMO, and chlorosome–baseplate–FMO–RC) are of great interest and should shed more light on chlorosome–baseplate interactions as well as electronic structure and EET dynamics of the BChl a –CsmA system.…”

On Excitation Energy Transfer within the Baseplate BChl a–CsmA Complex of Chloroflexus aurantiacus

“…Previously, the organization of CsmA proteins as a 2D crystalline lattice was directly observed via electron cryo-microscopy, and the structure of the CsmA protein has been determined by liquid-state NMR . Various models were proposed for the BChl a –CsmA dimer, but BChl dipole–dipole angles (30–125°) and center-to-center distances (7–18 Å) varied significantly. ,, Interestingly, the calculated magnitudes of the coupling matrix elements ( V ) have similar values of 30–35 cm –1 (assuming = 6.1 D). The high-resolution structure of the CsmA baseplate from C.…”

Optimal Energy Transfer in Light-Harvesting Systems

“…Secondly, unlike any other photosystems, the interior part of the chlorosome is entirely constituted by aggregated chromophores and does not present any protein scaffold within it. The assembled chromophores are in contact with the baseplate, an additional two-dimensional structure embedded in the chlorosome’s membrane which is mainly constituted of dimerized Bchl a-CsmA pigment-protein units [55]. The chlorosome constitutes the largest known photosystem, presenting an ellipsoidal shape whose dimensions are around 150 nm × 50 nm × 25 nm.…”