How Can We Predict Accurate Electrochromic Shifts for Biochromophores? A Case Study on the Photosynthetic Reaction Center.

Abhishek Sirohiwal,Dimitrios A Pantazis,Frank Neese

doi:10.1021/acs.jctc.0c01152

Abstract

Protein-embedded chromophores are responsible for light harvesting, excitation energy transfer, and charge separation in photosynthesis. A critical part of the photosynthetic apparatus are reaction centers (RCs), which comprise groups of (bacterio)chlorophyll and (bacterio)pheophytin molecules that transform the excitation energy derived from light absorption into charge separation. The lowest excitation energies of individual pigments (site energies) are key for understanding photosynthetic systems, and form a prime target for quantum chemistry. A major theoretical challenge is to accurately describe the electrochromic (Stark) shifts in site energies produced by the inhomogeneous electric field of the protein matrix. Here, we present large-scale quantum mechanics/molecular mechanics calculations of electrochromic shifts for the RC chromophores of photosystem II (PSII) using various quantum chemical methods evaluated against the domain-based local pair natural orbital (DLPNO) implementation of the similarity-transformed equation of motion coupled cluster theory with single and double excitations (STEOM-CCSD). We show that certain range-separated density functionals (ωΒ97, ωΒ97X-V, ωΒ2PLYP, and LC-BLYP) correctly reproduce RC site energy shifts with time-dependent density functional theory (TD-DFT). The popular CAM-B3LYP functional underestimates the shifts and is not recommended. Global hybrid functionals are too insensitive to the environment and should be avoided, while nonhybrid functionals are strictly nonapplicable. Among the applicable approximate coupled cluster methods, the canonical versions of CC2 and ADC(2) were found to deviate significantly from the reference results both for the description of the lowest excited state and for the electrochromic shifts. By contrast, their spin-component-scaled (SCS) and particularly the scale-opposite-spin (SOS) variants compare well with the reference DLPNO-STEOM-CCSD and the best range-separated DFT methods. The emergence of RC excitation asymmetry is discussed in terms of intrinsic and protein electrostatic potentials. In addition, we evaluate a minimal structural scaffold of PSII, the D1–D2–CytB559 RC complex often employed in experimental studies, and show that it would have the same site energy distribution of RC chromophores as the full PSII supercomplex, but only under the unlikely conditions that the core protein organization and cofactor arrangement remain identical to those of the intact enzyme.

Highlights

The input of energy into the biosphere is mediated by the conversion of sunlight to chemical energy in the form of separated charges, which drive the redox transformations of photosynthesis.[1−3] This process occurs in protein-embedded assemblies ofchlorophylls andpheophytins, the reaction centers (RCs) of biological photosystems
The origin and nature of the low-energy excited states inchlorophylls are typically conceptualized in the framework of the Gouterman model,[110,111] which attempts to describe the lowest energy absorption feature and the higherenergy feature in terms of four frontier orbitals, HOMO − 1, highest occupied molecular orbital (HOMO), lowest unoccupied molecular orbital (LUMO), and LUMO + 1
The majority of the contribution are derived from the HOMO → LUMO transition and secondarily from the HOMO − 1 → LUMO + 1 transition, both y-polarized in the idealized porphyrin parent system as opposed to the x-polarized HOMO → LUMO + 1 and HOMO − 1 → LUMO transitions

Summary

Introduction

The input of energy into the biosphere is mediated by the conversion of sunlight to chemical energy in the form of separated charges, which drive the redox transformations of photosynthesis.[1−3] This process occurs in protein-embedded assemblies of (bacterio)chlorophylls and (bacterio)pheophytins, the reaction centers (RCs) of biological photosystems. There are different types of RCs in biology They have extensive similarities, for example, in their two-branch arrangement of chromophores, and specific differences, for example, in the nature of terminal electron donors and acceptors, in the chemical nature of constituent pigments, and the functional asymmetry of the branches. The RC of the water-oxidizing PSII consists of chlorophyll a and pheophytin a molecules arranged in a pseudosymmetric fashion along two branches known as the D1 and D2 branches, from the conventional designation of the proteins that accommodate them.

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