Lattice Models for Protein Organization throughout Thylakoid Membrane Stacks

Abstract

Proteins in photosynthetic membranes can organize into patterned arrays that span the membrane's lateral size. Attractions between proteins in different layers of a membrane stack can play a key role in this ordering, as was suggested by microscopy and fluorescence spectroscopy and demonstrated by computer simulations of a coarse-grained model. The architecture of thylakoid membranes, however, also provides opportunities for interlayer interactions that instead disfavor the high protein densities of ordered arrangements. Here, we explore the interplay between these opposing driving forces and, in particular, the phase transitions that emerge in the periodic geometry of stacked thylakoid membrane disks. We propose a lattice model that roughly accounts for proteins' attraction within a layer and across the stromal gap, steric repulsion across the lumenal gap, and regulation of protein density by exchange with the stroma lamellae. Mean-field analysis and computer simulation reveal rich phase behavior for this simple model, featuring a broken-symmetry striped phase that is disrupted at both high and low extremes of chemical potential. The resulting sensitivity of microscopic protein arrangement to the thylakoid's mesoscale vertical structure raises intriguing possibilities for regulation of photosynthetic function.

Remembering the Work of Phillip L. Geissler: A Coda to His Scientific Trajectory

“…Mapping complicated phase behavior onto a lattice model was a particular passion of Phill's, and Ising models appeared in his work on hydrophobic solvation (18,19), nonequilibrium solvation (8), drying-mediated self-assembly (86), cation exchange in nanocrystals (109)(110)(111), and thylakoid membranes (72). Minimal models also provided Phill and his group with a lens through which to examine the dynamics of molecular systems driven away from equilibrium.…”

“…This finding led Phill and his group to explore whether the thylakoid's mesoscale vertical structure modulates such phase behavior through a minimally detailed lattice model of stacked discs that captured the alternating attractive and repulsive forces acting between vertically aligned membranes. Combining computer simulations with mean-field analysis, they (72) found that a modulated phase with long-range order would form under certain conditions (Figure 3c). Phill was keenly aware of the biological implications of phase transitions (73).…”

“…Understanding how phenomena at these disparate scales are coupled intrigued Phill and inspired him to devise novel Phill's work on biological membranes and the processes embedded within their milieu bridged macroscopic and molecular phenomena by combining simple coarse-grained models with atomistically detailed simulations: (a) Micrometer-scale membrane interfaces were modeled as an elastic mesh decorated by proteins (69), whereas (b) the exchange of individual lipids between membranes necessitated atomistic simulation (70,71). The influence of thylakoid's mesoscale vertical structure on protein organization was captured with (c) lattice models (72), whereas organization within the plane was recapitulated with (d) a nanoscale coarse-grained model (73). (e) Optimal molecular environments for positioning light-harvesting sites within protein scaffolds were investigated with atomistic models (74,75) Abbreviations: LHCII, light-harvesting complex II; PSII, photosystem II.…”

Coexistence of lipid phases in multilayer phospholipid films probed by Raman mapping

“…In some works, this effect is called “register effect”. Along with the simplicity of studying the composition of coexisting phases, multilayer planar structures are interesting as models of multilamellar biological structures, 23 such as thylakoid membranes of chloroplasts.…”

The Role of Periodic Structures in Light Harvesting

“…The mechanisms letting plants, algae, and bacteria generate fairly regular nanoscale structures are not yet fully explained. However, some remarkable works take into account the cellular genetic basis of the structural coloration of plants [ 9 ] and antenna proteins functions [ 10 ], as well as lattice models of organization, in stacks of thylakoids membranes [ 11 ]. There are several forms of structural color that are developed by surface diffraction gratings, multilayer reflectors, and helicoidal formations.…”