Functional Role of C α–H⋯O Hydrogen Bonds Between Transmembrane α-Helices in Photosystem I

Abstract

The crystal structure at 2.5 Å resolution of the membrane-intrinsic, homotrimeric photosystem I (PSI) isolated from the thermophilic cyanobacterium Synechococcus elongatus shows that each monomer is composed of 12 protein subunits of which nine are embedded in the membrane and feature a total of 34 transmembrane α-helices (TMH). Hence, PSI provides an ideal case to study “conventional” and C α–H⋯O hydrogen bonds between TMH engaged in intra- and intersubunit interactions. Of the total of 75 C α–H⋯O hydrogen bonds between TMHs, 72 are intrasubunit and only three are intersubunit. The two largest subunits PsaA and PsaB are each folded into 11 TMHs showing 29 and 24 intrasubunit C α–H⋯O hydrogen bonds, respectively, that are not distributed randomly but many of them flank chlorophyll a (Chl a) co-ordinating amino acids, suggesting stabilisation of these structural segments. As major constituent of the trimerisation domain, subunit PsaL is located next to the 3-fold axis relating the three monomers of PSI. PsaL features a unique number of 19 intrasubunit C α–H⋯O hydrogen bonds that connect two of its three TMHs but there are no intersubunit C α–H⋯O hydrogen bonds between the three PsaL. Of the three intersubunit C α–H⋯O hydrogen bonds, two are formed between PsaA and PsaB and one between PsaB and PsaM. The large number of 75 C α–H⋯O hydrogen bonds contrasts the 49 conventional hydrogen bonds, indicating that the former and van der Waals contacts determine association and orientation of TMHs in PSI.