A low complexity 3D model for heterogeneous wild type Chlorobaculum tepidum chlorosomes

Yuliya Miloslavinaa, Michael Reusb, Brijith Thomasa, Karthick Babu Sai Sankar Guptaa, Alfred R. Holzwarthb, Huub J.M. de Groota
aLeiden Institute of Chemistry, 2300 RA Leiden, The Netherlands; bMax-Planck-Institut für Chemische Energiekonversion Mülheim/Ruhr, Germany

Although chlorosomes from C. tepidum are intrinsically heterogeneous systems, they self-assemble in the same robust function-based structural framework, with limited, true complexity. Our main objective is to understand how self-assembly of pseudosymmetric BChl c syn-anti motifs leads to seamless concentric tubes and curved sheets. NMR data collected at 30 kHz MAS from an improved preparation of 13C-labeled chlorosomes reveal narrower signals than for earlier preparations, while the splitting in major and minor components, mainly for C-5 and C-7, is essentially independent of optical heterogeneity. T1ρ data provide for the first time a view on the hierarchical molecular dynamics in chlorosomes, where the part of the packing surrounding C-10 is more rigid than other parts of the ring, in particular carbons on rings I and IV.

To determine possible packing modes that are allowed by the experimental constraints from Cryo-EM and NMR, we performed ground-state molecular modeling using the DMol3 local orbital density functional and the CASTEP plane wave pseudopotential methods within the Materials Studio software, BIOVIA. 3D syn-anti models with periodic boundary conditions were resolved for wild type chlorosomes, including tails that further stabilize the structure. The main breakthrough is the realization of an ensemble of geometrically frustrated triangular lattices of BChls, where every third BChl cannot be opposite to both syn- and anti-BChls at the adjacent stack sites (Figure). This leads to degenerate ground states and competition between local and global order. We propose this as the core mechanism of domain formation in the chlorosome structure, leading to the gross heterogeneity on the supramolecular level detected in optical spectroscopy, while preserving local homogeneity on the NMR level. Major 70% cross peak in the doubling comes from domains of syn-anti BChl stacks and the minor 30% from all-syn or all-anti stacks, in transition regions between domains. In addition, all BChls across the domains can fulfill the same functional role and contribute to the antenna function equally well, which is the way nature keeps itself flexible for adaptation in a functionally robust chlorosome antenna structure with unique and superior light- harvesting properties.