Molecular Anatomy of Plant Photoprotective Switches: The Sensitivity of PsbS to the Environment, Residue by Residue

Nicoletta Liguori; Sara R.R. Campos; António M. Baptista; Roberta Croce

doi:10.1021/acs.jpclett.9b00437

Molecular Anatomy of Plant Photoprotective Switches: The Sensitivity of PsbS to the Environment, Residue by Residue

Nicoletta Liguori^*, Sara R.R. Campos, António M. Baptista, Roberta Croce

^*Corresponding author for this work

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

Abstract

Under strong sunlight, plants avoid photooxidation by quenching the excess absorbed energy. Quenching is triggered by PsbS, a membrane protein that is activated and deactivated by the light-dependent pH changes in the thylakoid lumen. The mechanism of action of this protein is unknown, but it was suggested that several glutamates act as pH sensors. However, the pK _a of glutamate is several pH units below the physiological values in the lumen. Thus, how can PsbS sense the pH of the lumen, and how does it respond to it? By applying a nonstandard molecular dynamics method that treats pH explicitly, we show that the lumen-exposed glutamates of PsbS have strongly shifted pK _a values and that such shifts are crucial for the pH sensitivity in physiological conditions. We also demonstrate that protonation drives a systematic unfolding of a region key for protein-protein interactions, indicating that PsbS response to pH is a functional conformational switch.

Original language	English
Pages (from-to)	1737-1742
Number of pages	6
Journal	Journal of Physical Chemistry Letters
Volume	10
Issue number	8
Early online date	25 Mar 2019
DOIs	https://doi.org/10.1021/acs.jpclett.9b00437
Publication status	Published - 18 Apr 2019

Funding

The authors are grateful to Vincenzo Mascoli and Mei Li for insightful discussions. This work is supported by The Netherlands Organization for Scientific Research (NWO), division Earth and Life science (ALW) via a Veni grant to N.L. and via a Vici grant to R.C.; by the ERC consolidator Grant 281341 (ASAP) to R.C.; by Project LISBOA-01-0145-FEDER-007660 (Microbiologia Molecular, Estrutural e Celular) funded by FEDER funds through COMPETE2020 - Programa Operacional Competitividade e Internacionalizaca̧ õ (POCI); and by national funds through FCT (Fundaca̧ õ para a Cienciâ e a Tecnologia). All the standard MD simulations in this work were carried out on the Dutch national e-infrastructure with the support of SURF Cooperative through a NWO grant to N.L. and R.C.

Funders	Funder number
COMPETE2020
Fundaca̧ õ para a Cienciâ e a Tecnologia
SURF
Seventh Framework Programme	281341
European Research Council	LISBOA-01-0145-FEDER-007660
Fundação para a Ciência e a Tecnologia
Nederlandse Organisatie voor Wetenschappelijk Onderzoek

Keywords

PsbS
Quenching
pKa
pH
Conformational switch
pH-sensing

UN SDGs

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

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10.1021/acs.jpclett.9b00437Licence: CC BY-NC-ND

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6477805

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Cite this

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title = "Molecular Anatomy of Plant Photoprotective Switches: The Sensitivity of PsbS to the Environment, Residue by Residue",

abstract = " Under strong sunlight, plants avoid photooxidation by quenching the excess absorbed energy. Quenching is triggered by PsbS, a membrane protein that is activated and deactivated by the light-dependent pH changes in the thylakoid lumen. The mechanism of action of this protein is unknown, but it was suggested that several glutamates act as pH sensors. However, the pK a of glutamate is several pH units below the physiological values in the lumen. Thus, how can PsbS sense the pH of the lumen, and how does it respond to it? By applying a nonstandard molecular dynamics method that treats pH explicitly, we show that the lumen-exposed glutamates of PsbS have strongly shifted pK a values and that such shifts are crucial for the pH sensitivity in physiological conditions. We also demonstrate that protonation drives a systematic unfolding of a region key for protein-protein interactions, indicating that PsbS response to pH is a functional conformational switch. ",

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author = "Nicoletta Liguori and Campos, {Sara R.R.} and Baptista, {Ant{\'o}nio M.} and Roberta Croce",

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AU - Liguori, Nicoletta

AU - Campos, Sara R.R.

AU - Baptista, António M.

AU - Croce, Roberta

PY - 2019/4/18

Y1 - 2019/4/18

N2 - Under strong sunlight, plants avoid photooxidation by quenching the excess absorbed energy. Quenching is triggered by PsbS, a membrane protein that is activated and deactivated by the light-dependent pH changes in the thylakoid lumen. The mechanism of action of this protein is unknown, but it was suggested that several glutamates act as pH sensors. However, the pK a of glutamate is several pH units below the physiological values in the lumen. Thus, how can PsbS sense the pH of the lumen, and how does it respond to it? By applying a nonstandard molecular dynamics method that treats pH explicitly, we show that the lumen-exposed glutamates of PsbS have strongly shifted pK a values and that such shifts are crucial for the pH sensitivity in physiological conditions. We also demonstrate that protonation drives a systematic unfolding of a region key for protein-protein interactions, indicating that PsbS response to pH is a functional conformational switch.

AB - Under strong sunlight, plants avoid photooxidation by quenching the excess absorbed energy. Quenching is triggered by PsbS, a membrane protein that is activated and deactivated by the light-dependent pH changes in the thylakoid lumen. The mechanism of action of this protein is unknown, but it was suggested that several glutamates act as pH sensors. However, the pK a of glutamate is several pH units below the physiological values in the lumen. Thus, how can PsbS sense the pH of the lumen, and how does it respond to it? By applying a nonstandard molecular dynamics method that treats pH explicitly, we show that the lumen-exposed glutamates of PsbS have strongly shifted pK a values and that such shifts are crucial for the pH sensitivity in physiological conditions. We also demonstrate that protonation drives a systematic unfolding of a region key for protein-protein interactions, indicating that PsbS response to pH is a functional conformational switch.

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Molecular Anatomy of Plant Photoprotective Switches: The Sensitivity of PsbS to the Environment, Residue by Residue

Abstract

Funding

Keywords

UN SDGs

Access to Document

Persistent URL (handle)

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Fingerprint

NWO regular project grant on national supercomputer Cartesius

NWO VENI grant

Cite this

Molecular Anatomy of Plant Photoprotective Switches: The Sensitivity of PsbS to the Environment, Residue by Residue

Abstract

Funding

Keywords

UN SDGs

Access to Document

Persistent URL (handle)

Other files and links

Fingerprint

Prizes

NWO regular project grant on national supercomputer Cartesius

NWO VENI grant

Cite this