Environment-dependent chlorophyll–chlorophyll charge transfer states in Lhca4 pigment–protein complex

Photosystem I (PSI) light-harvesting antenna complexes LHCI contain spectral forms that absorb and emit photons of lower energy than that of its primary electron donor, P700. The most red-shifted fluorescence is associated with the Lhca4 complex. It has been suggested that this red emission is related to the inter-chlorophyll charge transfer (CT) states. In this work we present a systematic quantum-chemical study of the CT states in Lhca4, accounting for the influence of the protein environment by estimating the electrostatic interactions. We show that significant energy shifts result from these interactions and propose that the emission of the Lhca4 complex is related not only to the previously proposed a603+–a608− state, but also to the a602+–a603− state. We also investigate how different protonation patterns of protein amino acids affect the energetics of the CT states.

5 Other Supplementary data included in the Supplementary_Material.xlsx file

Worksheet Data presented
Table S1 Net charges of the protein amino acids Table S2 Atomic coordinates and partial charges of Chl a602, used as a reference for all Chl a pigments Table S3 Atomic coordinates and partial charges of Chl b605, used as a reference for all Chl b pigments Table S4 Atomic coordinates and partial charges of Chl a601 in its ground state.

Table S5
Atomic coordinates and partial charges of Chl a601 in its first excited state state.

Table S6
Atomic coordinates and partial charges of Chl a602 in its ground state.

Table S7
Atomic coordinates and partial charges of Chl a602 in its first excited state state.

Table S8
Atomic coordinates and partial charges of Chl a603 in its ground state.

Table S9
Atomic coordinates and partial charges of Chl a603 in its first excited state state.

Table S10
Atomic coordinates and partial charges of Chl a604 in its ground state.

Table S11
Atomic coordinates and partial charges of Chl a604 in its first excited state state.

S8
Worksheet Data presented

Table S12
Atomic coordinates and partial charges of Chl a608 in its ground state.
Table S13 Atomic coordinates and partial charges of Chl a608 in its first excited state state.

Table S14
Atomic coordinates and partial charges of Chl a609 in its ground state.

Table S15
Atomic coordinates and partial charges of Chl a609 in its first excited state state.

Table S16
Atomic coordinates and partial charges of Chl a610 in its ground state.

Table S17
Atomic coordinates and partial charges of Chl a610 in its first excited state state.

Table S18
Atomic coordinates and partial charges of Chl a611 in its ground state.
Table S19 Atomic coordinates and partial charges of Chl a611 in its first excited state state.
Table S20 Atomic coordinates and partial charges of Chl a612 in its ground state.
Table S21 Atomic coordinates and partial charges of Chl a612 in its first excited state state.

Table S22
Atomic coordinates and partial charges of Chl a613 in its ground state.
Table S23 Atomic coordinates and partial charges of Chl a613 in its first excited state state.

Table S24
Atomic coordinates and partial charges of Chl a614 in its ground state.

Table S25
Atomic coordinates and partial charges of Chl a614 in its first excited state state.

Table S26
Atomic coordinates and partial charges of Chl b605 in its ground state.

Table S27
Atomic coordinates and partial charges of Chl b605 in its first excited state state.

Table S28
Atomic coordinates and partial charges of Chl b606 in its ground state.

Table S29
Atomic coordinates and partial charges of Chl b606 in its first excited state state.

Table S30
Atomic coordinates and partial charges of Chl b607 in its ground state.
Table S31 Atomic coordinates and partial charges of Chl b607 in its first excited state state.
Table S32 Atomic coordinates and partial charges of Chl b615 in its ground state.
Table S33 Atomic coordinates and partial charges of Chl b615 in its first excited state state.

Table S34
Atomic coordinates and partial charges of dimer a601-a610 in its ground state.

Table S35
Atomic coordinates and partial charges of dimer a601-a610 in its first excited state.

Table S36
Atomic coordinates and partial charges of dimer a601-a610 in its fifth excited (CT) state.

Table S37
Atomic coordinates and partial charges of dimer a601-a610 in its sixth excited (CT) state.

Table S38
Atomic coordinates and partial charges of dimer a602-a603 in its ground state.

Table S39
Atomic coordinates and partial charges of dimer a602-a603 in its first excited state.

Table S40
Atomic coordinates and partial charges of dimer a602-a603 in its fifth excited (CT) state.

Table S41
Atomic coordinates and partial charges of dimer a602-a603 in its sixth excited (CT) state.

Table S42
Atomic coordinates and partial charges of dimer a603-a608 in its ground state.

S9
Worksheet Data presented Table S43 Atomic coordinates and partial charges of dimer a603-a608 in its first excited state.

Table S44
Atomic coordinates and partial charges of dimer a603-a608 in its sixth excited (CT) state.

Table S45
Atomic coordinates and partial charges of dimer a608-a614 in its ground state.

Table S46
Atomic coordinates and partial charges of dimer a608-a614 in its first excited state.
Table S47 Atomic coordinates and partial charges of dimer a608-a614 in its fifth excited (CT) state.

Table S48
Atomic coordinates and partial charges of dimer a608-a614 in its sixth excited (CT) state.

Table S49
Atomic coordinates and partial charges of dimer a604-b605 in its ground state.
Table S50 Atomic coordinates and partial charges of dimer a604-b605 in its first excited state.
Table S51 Atomic coordinates and partial charges of dimer a604-b605 in its fifth excited (CT) state.

Table S52
Atomic coordinates and partial charges of dimer a604-b605 in its sixth excited (CT) state.
Table S53 Atomic coordinates and partial charges of dimer a604-b605 in its eighth excited (CT) state.

Table S54
Atomic coordinates and partial charges of dimer a608-b607 in its ground state.

Table S55
Atomic coordinates and partial charges of dimer a608-b607 in its first excited state.

Table S56
Atomic coordinates and partial charges of dimer a608-b607 in its fifth excited (CT) state.

Table S57
Atomic coordinates and partial charges of dimer a609-b607 in its ground state.

Table S58
Atomic coordinates and partial charges of dimer a609-b607 in its first excited state.

Table S59
Atomic coordinates and partial charges of dimer a609-b607 in its fifth excited (CT) state.

Table S60
Atomic coordinates and partial charges of dimer b607-b615 in its ground state.

Table S61
Atomic coordinates and partial charges of dimer b607-b615 in its first excited state.
Table S62 Atomic coordinates and partial charges of dimer b607-b615 in its seventh excited (CT) state.
Table S63 Atomic coordinates and partial charges of dimer a609-a611 in its ground state.
Table S64 Atomic coordinates and partial charges of dimer a609-a611 in its first excited state.

Table S65
Atomic coordinates and partial charges of dimer a609-a611 in its fifth excited (CT) state.

Table S66
Atomic coordinates and partial charges of dimer a610-a611 in its ground state.

Table S67
Atomic coordinates and partial charges of dimer a610-a611 in its first excited state.

Table S68
Atomic coordinates and partial charges of dimer a610-a611 in its fifth excited (CT) state.

Table S69
Atomic coordinates and partial charges of dimer a610-a611 in its sixth excited (CT) state.

Table S70
Atomic coordinates and partial charges of dimer a612-a613 in its ground state.

Table S71
Atomic coordinates and partial charges of dimer a612-a613 in its first excited state.

Table S72
Atomic coordinates and partial charges of dimer a612-a613 in its fifth excited (CT) state.

Table S73
Atomic coordinates and partial charges of dimer a612-a613 in its sixth excited (CT) state.

S10
Worksheet Data presented

Table S74
Atomic coordinates and partial charges of dimer a612-a613 in its seventh excited (CT) state.

Table S75
Atomic coordinates and partial charges of violaxanthin (XAT617) in its ground state.

Table S76
Atomic coordinates and partial charges of lutein (LUT616) in its ground state.

Table S77
Atomic coordinates and partial charges of beta carotene (BCR618) in its ground state.

Figure S1 .
Figure S1.The difference of energy shifts calculated in estimated protonation environment and all non-standard protonation environments for all Qy energies of monomers.

Table S -
II. Partial charges of carotenoids LUT, XAT and BCR in their ground state based on fit of the electrostatic potential.The charges of hydrogen atoms are set to 0.

Table S -
III. pKa values of titratable amino acids in Lhca4 protein chain.The values were obtained considering neutral pH using PROPKA 3 tool.

Table S -
IV.The comparison of static and transition dipole moments for the first eight excited states of selected dimers.The last two columns give the sum of Mulliken partial charges for each pigment of the dimer.
4 Monomer energy shift changes in various non-standard protonation patterns