Publication: Light Harvesting Complex and Chlorophyll Aggregation in Membranes using Molecular Dynamics Simulations
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2025-04-09
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Indian Institute of Technology, Jodhpur
Abstract
The light-harvesting complex (LHCII), a pigmented protein trimer embedded in thylakoid membranes of plants, captures energy from sunlight through its pigments primarily chlorophyll, and transfers it to the photosynthetic reaction center during photosynthesis. Chlorophyll molecules reside around the LHCII trimer in a belt-like configuration. The conserved composition of the thylakoid membrane which hosts protein complexes and cofactors in plants is found to be essential for light harvesting and pivotal in non-photochemical quenching (NPQ), the process by which excess energy from sunlight is dissipated as heat to protect photosynthetic organisms from photodamage. The chlorophyll derivatives bound in the membrane are important in designing artificial photosynthetic materials. The properties of chlorophylls, such as energy conversion and electron transfer depend on how the chlorophylls are assembled in thylakoid membranes. The membrane comprises different types of lipids with different degrees of unsaturation based on the number and their positions along the alkyl chains. Tail unsaturation plays an important role in photosynthesis, forming different cellular structures, adaptation to environmental stresses, and so on. However, the relation between the tail unsaturation to the stability of chlorophyll aggregate is unexplored till now. The role of the lipidome of thylakoid in regulating the harvesting is unclear. The molecular origin of the stability of the trimeric complex in the membrane remains elusive to date. Thus, the current thesis proceeds to investigate the origin of the structural integrity of LHCII in lipid membranes, thermodynamics, dynamics of chlorophyll aggregation, and the role of lipids on the aggregation using all-atom (AA) and coarse-grained (CG) molecular dynamics simulations. AA molecular dynamics (MD) simulations of LHCII are carried out in a dipalmitoylphosphatidylcholine (DPPC) membrane at 323 K. Central associations of chlorophyll a (CLA) pigment molecules near the LHCII are attributed to conserved coordination between the CLA and specific residues of the first helix of a chain. The residue forms a salt-bridge with the fourth helix of the same chain of the trimer, not of the monomer. In an earlier experiment, three residues (WYR) at each chain of the trimer have been found indispensable for the trimerization and referred to as the trimerization motif. Our simulations show that the residues of the trimerization motif are connected to the lipids or pigments by a chain of interactions rather than direct contact. Synergistic effects of sequentially located hydrogen bonds and salt bridges within monomers of the trimer keep the trimer conformation stable in association with the pigments or the lipids. CG molecular dynamics simulations of CLA are carried out in plant thylakoid membranes at 293 K by varying the total lipid-to-CLA ratio using our previously derived CG model of CLA and MARTINI force fields for lipids. Our simulations show that CLA molecules dynamically form aggregates that break and reform, corroborated by earlier fluorescence quenching experiments. The number of aggregates increases with an increasing concentration of CLA. Selective lipids promote the formation of CLA aggregates governed by van der Waals interactions in plant thylakoid membranes. Less unsaturated lipids reside near the aggregate, promoting increased order and efficient packing. Conversely, higher unsaturated lipids are depleted from the aggregate, imparting flexibility to the membrane. Such preferential locations of lipids around the aggregates result in increasing lateral heterogeneity in the order parameter and density with increasing CLA concentrations. This induces more undulation in membranes, resulting in a lower bending modulus and area compressibility. To understand the role of lipid compositions in the stability of CLA aggregates, the potential of mean force of a CLA dimer is calculated in the presence of the thylakoid and the bilayers comprising either the least or the highest unsaturated lipids by using CG MD simulations. The thylakoid membrane enhances the stability of the CLA dimer compared to the least and highest unsaturated membranes. Lipid mixing, rather than lipid unsaturation, plays a critical role in facilitating CLA dimerization by modulating the membrane microenvironment through stronger lipid-lipid interactions. The microenvironment of the selective lipids in the vicinity of the aggregated CLA remains conserved as in the LHCII trimer which suggests CLA as the origin of the lipid fingerprints in thylakoid. The contact lifetime and waiting time distributions of CLA dimers exhibit the existence of multiple time scales, including most populated fast time scales and less populated slow time scales. The survival probability of CLA dimers follows a non-exponential decay with multiple residence time scales which leads to a time-dependent rate, unlike conventional rate theory. Such non-exponential decay of dimer survival is a manifestation of dynamic disorder resulting from coupling between time scales of dimer formation and higher-order aggregates. In summary, the study indicates that the conformation of the LHCII trimer, along with the CLA association and the microenvironment of the selective lipids in its vicinity, as a whole, can be instrumental for the stability and functions of the photosynthetic machinery. The results from the study can be extended and useful in understanding the role of the CLA binding LHCII or their aggregation hosted by thylakoid on the optimal photosynthetic function by enhancing light absorption and by dissipating excess energy. Our research provides the foundation for a better understanding of more complex biophysical phenomena, such as NPQ, in the future
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Saini, Renu(2019).Light Harvesting Complex and Chlorophyll Aggregation in Membranes using Molecular Dynamics Simulations (Doctor's thesis). Indian Institute of Technology Jodhpur