An Unexpected Water Channel in the Light-Harvesting\nComplex of a Diatom: Implications for the Switch between Light Harvesting\nand Photoprotection

Many important processes\nin cells depend on the transfer of protons\nthrough water wires embedded in transmembrane proteins. Herein, we\nhave performed more than 55 μs all-atom simulations of the\nlight-harvesting complex of a diatom, i.e., the fucoxanthin and chlorophyll\na/c binding protein (FCP) from the marine diatom Phaeodactylum\ntricornutum. Diatoms are unique models to study natural\nphotosynthesis as they exert an efficient light-harvesting machinery\nwith a robust pH-dependent photoprotective mechanism. The present\nstudy reports on the dynamics of an FCP monomer, a dimer, and a tetramer\nat varying pH values. Surprisingly, we have identified at low pH a\nwater channel across FCP that selectively hydrates and protonates\nthe acrylate of a Chl-c2 pigment located in the middle of the membrane.\nThese results are further supported by QM/MM calculations and steered\nMD simulations on the proton dynamics. It is shown that proton hopping\nevents between the lumenal and stromal sides of the membrane through\nthe observed water channel are highly disfavored. This hindrance is\ndue to the presence of residues Arg31 and Lys82 close to the acrylate,\nalong with an hydronium desolvation penalty that shows close similarities\nto the water conductance in aquaporins. Furthermore, we provide strong\nevidence that this identified water channel is governing the transition\nbetween light-harvesting and photoprotective states of the major FCP\ncomplex in the diatom P. tricornutum.