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Title: Revealing the Dynamics of Thylakoid Membranes in Living Cyanobacterial Cells

Abstract

Cyanobacteria are photosynthetic prokaryotes that make major contributions to the production of the oxygen in the Earth atmosphere. The photosynthetic machinery in cyanobacterial cells is housed in flattened membrane structures called thylakoids. The structural organization of cyanobacterial cells and the arrangement of the thylakoid membranes in response to environmental conditions have been widely investigated. However, there is limited knowledge about the internal dynamics of these membranes in terms of their flexibility and motion during the photosynthetic process. Here, we present a direct observation of thylakoid membrane undulatory motion in vivo and show a connection between membrane mobility and photosynthetic activity. High-resolution inelastic neutron scattering experiments on the cyanobacterium Synechocystis sp. PCC 6803 assessed the flexibility of cyanobacterial thylakoid membrane sheets and the dependence of the membranes on illumination conditions. Moreover, we observed softer thylakoid membranes in the dark that have three-to four fold excess mobility compared to membranes under high light conditions. Finally, our analysis indicates that electron transfer between photosynthetic reaction centers and the associated electrochemical proton gradient across the thylakoid membrane result in a significant driving force for excess membrane dynamics. These observations provide a deeper understanding of the relationship between photosynthesis and cellular architecture.

Authors:
 [1];  [2];  [3];  [2];  [3];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Sciences Directorate (NScD
  3. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). High Flux Isotope Reactor (HFIR); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1259841
Alternate Identifier(s):
OSTI ID: 1261505
Grant/Contract Number:  
SC0001035; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Stingaciu, Laura-Roxana, O’Neill, Hugh, Liberton, Michelle, Urban, Volker S., Pakrasi, Himadri B., and Ohl, Michael. Revealing the Dynamics of Thylakoid Membranes in Living Cyanobacterial Cells. United States: N. p., 2016. Web. doi:10.1038/srep19627.
Stingaciu, Laura-Roxana, O’Neill, Hugh, Liberton, Michelle, Urban, Volker S., Pakrasi, Himadri B., & Ohl, Michael. Revealing the Dynamics of Thylakoid Membranes in Living Cyanobacterial Cells. United States. https://doi.org/10.1038/srep19627
Stingaciu, Laura-Roxana, O’Neill, Hugh, Liberton, Michelle, Urban, Volker S., Pakrasi, Himadri B., and Ohl, Michael. Thu . "Revealing the Dynamics of Thylakoid Membranes in Living Cyanobacterial Cells". United States. https://doi.org/10.1038/srep19627. https://www.osti.gov/servlets/purl/1259841.
@article{osti_1259841,
title = {Revealing the Dynamics of Thylakoid Membranes in Living Cyanobacterial Cells},
author = {Stingaciu, Laura-Roxana and O’Neill, Hugh and Liberton, Michelle and Urban, Volker S. and Pakrasi, Himadri B. and Ohl, Michael},
abstractNote = {Cyanobacteria are photosynthetic prokaryotes that make major contributions to the production of the oxygen in the Earth atmosphere. The photosynthetic machinery in cyanobacterial cells is housed in flattened membrane structures called thylakoids. The structural organization of cyanobacterial cells and the arrangement of the thylakoid membranes in response to environmental conditions have been widely investigated. However, there is limited knowledge about the internal dynamics of these membranes in terms of their flexibility and motion during the photosynthetic process. Here, we present a direct observation of thylakoid membrane undulatory motion in vivo and show a connection between membrane mobility and photosynthetic activity. High-resolution inelastic neutron scattering experiments on the cyanobacterium Synechocystis sp. PCC 6803 assessed the flexibility of cyanobacterial thylakoid membrane sheets and the dependence of the membranes on illumination conditions. Moreover, we observed softer thylakoid membranes in the dark that have three-to four fold excess mobility compared to membranes under high light conditions. Finally, our analysis indicates that electron transfer between photosynthetic reaction centers and the associated electrochemical proton gradient across the thylakoid membrane result in a significant driving force for excess membrane dynamics. These observations provide a deeper understanding of the relationship between photosynthesis and cellular architecture.},
doi = {10.1038/srep19627},
journal = {Scientific Reports},
number = ,
volume = 6,
place = {United States},
year = {Thu Jan 21 00:00:00 EST 2016},
month = {Thu Jan 21 00:00:00 EST 2016}
}

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Diverse hydrocarbon biosynthetic enzymes can substitute for olefin synthase in the cyanobacterium Synechococcus sp. PCC 7002
journal, February 2019


Influence of Chemically Disrupted Photosynthesis on Cyanobacterial Thylakoid Dynamics in Synechocystis sp. PCC 6803
journal, April 2019

  • Stingaciu, Laura-Roxana; O’Neill, Hugh M.; Liberton, Michelle
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Macroorganisation and flexibility of thylakoid membranes
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Charge regulation radically modifies electrostatics in membrane stacks
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The Role of Slr0151, a Tetratricopeptide Repeat Protein from Synechocystis sp. PCC 6803, during Photosystem II Assembly and Repair
journal, May 2016


Charge regulation radically modifies electrostatics in membrane stacks
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