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Interactions Determining the Structural Integrity of the Trimer of Plant Light Harvesting Complex in Lipid Membranes

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Abstract

The structural basis for the stability of the trimeric form of the light harvesting complex (LHCII), a pigmented protein from green plants pivotal for photosynthesis, remains elusive till date. The protein embedded in a dipalmitoylphosphatidylcholine (DPPC) lipid membrane is investigated using all-atom molecular dynamics simulations to find out the interactions responsible for the structural integrity of the trimer and its relation to antenna function. Central association of chlorophyll a (CLA) molecules near the LHCII chains is attributed to a conserved coordination between the Mg of CLA and the oxygen of a specific residue 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 trimerization motif. We find that the residues of the trimerization motif are connected to the lipids or pigments by a chain of interactions rather than a 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. These interactions are exclusively present in the pigmented trimer and not present in the monomer or in the unpigmented trimer. Thus, our results provide a molecular basis for the inherent stability of the LHCII trimer in a lipid membrane and explain many pre-existing experimental data.

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Data Availability Statement

Data will be available upon reasonable request.

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Acknowledgements

This project had been started while the authors (AD, CG, CP) were affiliated with the Max Planck Institute for Polymer Research as part of the Collaborative Research Center (SFB 625) in Mainz: “From Single Molecules to Nanoscopically Structured Materials.” We would like to thank Kurt Kremer and Harald Paulsen for many inspiring discussions. RS and AD are thankful to Arpita Srivastava for her help during the preparation of the manuscript.

Funding

AD, CG, and CP are thankful to SFB 625 and the fellowship program of the Max Planck Society for financial assistance. AD is thankful to the grant SERB CRG/2019/000106 and IITJ SEED grant IITJ/SEED/20140016 for funding.

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Authors and Affiliations

  1. Indian Institute of Technology Jodhpur, Jodhpur, 342037, India

    Renu Saini & Ananya Debnath

  2. University of Konstanz, Konstanz, Germany

    Christoph Globisch, Leon Franke & Christine Peter

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  1. Renu Saini
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  2. Christoph Globisch
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  3. Leon Franke
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  4. Christine Peter
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  5. Ananya Debnath
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Contributions

CP has conceived the project. RS and AD have performed the simulations. RS, CG, LF, and AD have performed the analyses. RS, CG, CP, and AD have written the manuscript.

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Correspondence to Ananya Debnath.

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Saini, R., Globisch, C., Franke, L. et al. Interactions Determining the Structural Integrity of the Trimer of Plant Light Harvesting Complex in Lipid Membranes. J Membrane Biol 254, 157–173 (2021). https://doi.org/10.1007/s00232-020-00162-x

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