Surface charge dynamics in photosynthetic membranes and its structural consequences

Bart van Oort; Sujith Puthiyaveetil; Helmut Kirchhoff

doi:10.1038/nplants.2017.20

Surface charge dynamics in photosynthetic membranes and its structural consequences

Bart van Oort, Sujith Puthiyaveetil, Helmut Kirchhoff

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

The strict stacking of plant photosynthetic membranes into granal structures plays a vital role in energy conversion. The molecular forces that lead to grana stacking, however, are poorly understood. Here we evaluate the interplay between repulsive electrostatic (Fel) and attractive van der Waals (FvdWaals) forces in grana stacking. In contrast to previous reports, we find that the physicochemical balance between attractive and repulsive forces fully explains grana stacking. Extending the force balance analysis to lateral interactions within the oxygen-evolving photosystem II (PSII)–light harvesting complex II (LHCII) supercomplex reveals that supercomplex stability is very sensitive to Fel changes. Fel is highly dynamic, increasing up to 1.7-fold on addition of negative charges by phosphorylation of grana-hosted proteins. We show that this leads to specific destabilization of the supercomplex, and that changes in Fel have contrasting effects on vertical stacking and lateral intramembrane organization. This enables discrete biological control of these central structural features.

Original language	English
Article number	10.1038/nplants.2017.20
Pages (from-to)	17020
Journal	Nature Plants
Volume	2
DOIs	https://doi.org/10.1038/nplants.2017.20
Publication status	Published - 6 Mar 2017

Funding

This work was supported by grants to H.K. from the National Science Foundation (NSF-MCB-1616982) the US Department of Energy (DE-SC 0017160), the US Department of Agriculture (ARC grant WNP00775) and Washington State University. B.v.O. acknowledges financial support by the Netherlands Organisation for Scientific Research (NWO) through a Veni grant to B.v.O and a Vici grant to R. Croce. We thank P. Malý for help with calculating intermembrane electrostatic force. Finally, we thank G. Schoenknecht (Stillwater, OK, USA) and R. Fristedt (Amsterdam, The Netherlands) for their valuable comments and helpful suggestions.

Funders	Funder number
National Science Foundation	NSF-MCB-1616982, 1616982
U.S. Department of Energy	DE-SC 0017160
U.S. Department of Agriculture
Washington State University
Automotive Research Center	WNP00775
Nederlandse Organisatie voor Wetenschappelijk Onderzoek

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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title = "Surface charge dynamics in photosynthetic membranes and its structural consequences",

abstract = "The strict stacking of plant photosynthetic membranes into granal structures plays a vital role in energy conversion. The molecular forces that lead to grana stacking, however, are poorly understood. Here we evaluate the interplay between repulsive electrostatic (Fel) and attractive van der Waals (FvdWaals) forces in grana stacking. In contrast to previous reports, we find that the physicochemical balance between attractive and repulsive forces fully explains grana stacking. Extending the force balance analysis to lateral interactions within the oxygen-evolving photosystem II (PSII)–light harvesting complex II (LHCII) supercomplex reveals that supercomplex stability is very sensitive to Fel changes. Fel is highly dynamic, increasing up to 1.7-fold on addition of negative charges by phosphorylation of grana-hosted proteins. We show that this leads to specific destabilization of the supercomplex, and that changes in Fel have contrasting effects on vertical stacking and lateral intramembrane organization. This enables discrete biological control of these central structural features.",

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Surface charge dynamics in photosynthetic membranes and its structural consequences

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