How the Electron-Transfer Cascade is Maintained in Chlorophyll- <i>d</i> Containing Photosystem I

Photosystem I (PSI) from <i>Acaryochloris marina</i> utilizes chlorophyll <i>d</i> (Chl<i>d</i>) with a formyl group as its primary pigment, which is more red-shifted than chlorophyll <i>a</i> (Chl<i>a</i>) in PSI from <i>Thermosynechococcus elongatus</i>. Using the cryo-electron microscopy structure and solving the linear Poisson-Boltzmann equation, here we report the redox potential (<i>E</i>_m) values in <i>A. marina</i> PSI. The <i>E</i>_m(Chl<i>d</i>) values at the paired chlorophyll site, [P_AP_B], are nearly identical to the corresponding <i>E</i>_m(Chl<i>a</i>) values in <i>T. elongatus</i> PSI, despite Chl<i>d</i> having a 200 mV lower reduction power. The accessory chlorophyll site, A_-1, in the B branch exhibits an extensive H-bond network with its ligand water molecule, contributing to <i>E</i>_m(A_-1B) being lower than <i>E</i>_m(A_-1A). The substitution of pheophytin <i>a</i> (Pheo<i>a</i>) with Chl<i>a</i> at the electron acceptor site, A₀, decreases <i>E</i>_m(A₀), resulting in an uphill electron transfer from A_-1. The impact of the A_-1 formyl group on <i>E</i>_m(A₀) is offset by the reorientation of the A₀ ester group. It seems likely that Pheo<i>a</i> is necessary for <i>A. marina</i> PSI to maintain the overall electron-transfer cascade characteristic of PSI in its unique light environment.