Metal cations modulate the bacteriochlorophyll–protein interaction in the light-harvesting 1 core complex from Thermochromatium tepidum

Abstract

The light-harvesting 1 reaction center (LH1-RC) complex from Thermochromatium (Tch.) tepidum exhibits unusual Q(y) absorption by LH1 bacteriochlorophyll-a (BChl-a) molecules at 915nm, and the transition energy is finely modulated by the binding of metal cations to the LH1 polypeptides. Here, we demonstrate the metal-dependent interactions between BChl-a and the polypeptides within the intact LH1-RC complexes by near-infrared Raman spectroscopy. The wild-type LH1-RC (B915) exhibited Raman bands for the C3-acetyl and C13-keto CO stretching modes at 1637 and 1675cm(-1), respectively. The corresponding bands appeared at 1643 and 1673cm(-1) when Ca(2+) was biosynthetically replaced with Sr(2+) (B888) or at 1647 and 1669cm(-1) in the mesophilic counterpart, Allochromatium vinosum. These results indicate the significant difference in the BChl-polypeptide interactions between B915 and B888 and between B915 and the mesophilic counterpart. The removal of the original metal cations from B915 and B888 resulted in marked band shifts of the C3-acetyl/C13-carbonyl νCO modes to ~1645/~1670cm(-1), supporting a model in which the metal cations are involved in the fine-tuning of the hydrogen bonding between the BChl-a and LH1-polypeptides. Interestingly, the interaction modes were almost identical between the Ca(2+)-depleted B915 and Sr(2+)-depleted B888 and between B915 and Ca(2+)-substituted B888, despite the significant differences in their LH1 Q(y) peak positions and the denaturing temperatures, as revealed by differential scanning calorimetry. These results suggest that not only the BChl-polypeptide interactions but some structural origin may be involved in the unusual Q(y) red-shift and the enhanced thermal stability of the LH1-RC complexes from Tch. tepidum.

Cryo-EM structure of a Ca2+-bound photosynthetic LH1-RC complex containing multiple αβ-polypeptides

“…This Ca 2+ -binding effect has been demonstrated to contribute to the large redshifts of the LH1-Q y transitions in both Tch. tepidum 9 , 14 , 18 – 20 and Trv . strain 970 16 .…”

“…Among the many factors, hydrogen bonding between BChl a and its surrounding proteins has a direct effect on the lowest-energy transition, and one of the most effective methods for detecting the hydrogen bonds is resonance Raman spectroscopy. There is a linear relationship between the redshift of the Raman band in the BChl a C3-acetyl stretching mode and the redshift in the LH absorption maximum 7 , 18 , 34 , 35 . The redshift of the Raman band observed at 1621 cm −1 for the Trv .…”

“…Much of the insight gained from the thoroughly investigated Tch. tepidum LH1-RC 9 – 11 , 14 , 15 , 18 , 20 , 28 – 30 has paved the way for understanding the structural basis of the spectroscopic behavior of the Trv . strain 970 LH1-RC because the Ca 2+ -binding sites are similar in the two complexes.…”

Probing structure–function relationships in early events in photosynthesis using a chimeric photocomplex

“…The near-infrared Raman results show that the hydrogen-bonding interactions between the BChl a C3-acetyl group and LH1 polypeptides in the native Tch. tepidum (24) are also major factors regulating the Q y transition of the expressed LH1 complexes.…”

Spectral Properties of Chlorophyll f in the B800 Cavity of Light‐harvesting Complex 2 from the Purple Photosynthetic Bacterium Rhodoblastus acidophilus

“…The hydrogen bonding between the carbonyl groups of (B)Chl pigments and the neighboring amino acid residues in light‐harvesting proteins is an important factor in fine‐tuning of the absorption energies of (B)Chl pigments (8–11). Such interactions have been extensively studied for the 3‐acetyl group of BChl a in bacterial light‐harvesting proteins, such as light‐harvesting complex 1 (12–17), light‐harvesting complex 2 (LH2) (12,18–22), light‐harvesting complex 3 (12,19,23) and Fenna–Matthews–Olson proteins (24–26).…”