Excitonic Energy Landscape of the Y16F Mutant of the Chlorobium tepidum Fenna–Matthews–Olson (FMO) Complex: High Resolution Spectroscopic and Modeling Studies

Abstract

We report high-resolution (low-temperature) absorption, emission, and nonresonant/resonant hole-burned (HB) spectra and results of excitonic calculations using a non-Markovian reduced density matrix theory (with an improved algorithm for parameter optimization in heterogeneous samples) obtained for the Y16F mutant of the Fenna-Matthews-Olson (FMO) trimer from the green sulfur bacterium Chlorobium tepidum. We show that the Y16F mutant is a mixture of FMO complexes with three independent low-energy traps (located near 817, 821, and 826 nm), in agreement with measured composite emission and HB spectra. Two of these traps belong to mutated FMO subpopulations characterized by significantly modified low-energy excitonic states. Hamiltonians for the two major subpopulations (Sub and Sub) provide new insight into extensive changes induced by the single-point mutation in the vicinity of BChl 3 (where tyrosine Y16 was replaced with phenylalanine F16). The average decay time(s) from the higher exciton state(s) in the Y16F mutant depends on frequency and occurs on a picosecond time scale.

How the Protein Environment Can Tune the Energy, the Coupling, and the Ultrafast Dynamics of Interacting Chlorophylls: The Example of the Water-Soluble Chlorophyll Protein

“…In conclusion, we have demonstrated that the effect of the protein scaffold in pigment–protein complexes is not limited to variations of the site energies of the pigments, as largely documented in the literature, ,− ,,− but that the establishment of specific and directional interactions can have very strong consequences for the electronic coupling and for the ultrafast dynamics of pigment–protein complexes as well. This is a particularly important finding because beyond having characterized this behavior in the WSCP, it implies the possibility of tuning the photophysics and the transport properties of multichromophores by engineering specific interactions with the surroundings.…”

“…Biological systems, such as light-harvesting complexes, are characterized by optimized structures where the protein scaffold acts on the active molecules, finely tuning their surroundings and modulating their properties and functionalities. Numerous studies have addressed the contributions of individual amino acids to modulating the spectroscopic properties of bound chromophores, recognizing that they may act either by determining their 3D arrangement, − thus affecting their interchromophore interactions, or by modifying their site energy. − In several instances, these chromophore tunings have been achieved by means of hydrogen (H) bonds. ,− ,, …”

“…3−17 In several instances, these chromophore tunings have been achieved by means of hydrogen (H) bonds. 2,[5][6][7][8][9]16,17 Nevertheless, several details of the complex interplay between the active molecules and the protein environment at the molecular level are not fully clarified, and how to replicate the same mechanisms in artificial systems is still open to investigation. 18−20 In this context, the water-soluble chlorophyll protein (WSCP) represents an ideal model system to investigate this kind of interaction more deeply.…”

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).…”

How water-mediated hydrogen bonds affect chlorophyll a/b selectivity in Water-Soluble Chlorophyll Protein

“…This latter role is of paramount relevance for proteins involved in the photosynthetic process, as they need to bind numerous pigments, such as chlorophylls (Chls), in a precise three-dimensional arrangement to effectively harvest and utilize incoming light 6 . Numerous mutational studies have been performed on photosynthetic proteins, that helped to highlight the role of individual H-bonds in determining the spectroscopic properties of the bound pigments 7–14 . Beside modulating the properties of the bound Chls 7–10,15 , the presence of an appropriate H-bond donor in close proximity to the C-7 1 atom of the Chls (see Fig.…”