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. 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. We observed softer thylakoid membranes in the dark that have three-to four fold excess mobility compared to membranes under high light conditions. 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.

Highlights

  • Among non-invasive techniques, Small Angle Neutron Scattering (SANS) in combination with other methods[8,9,10,11,12] is able to provide spatially averaged structural information about membranes systems under different experimental conditions, in algal cells[8,9,10,11] and in isolated thylakoid membrane sistems[11,12]

  • We observe the mobility of thylakoid membranes in live cyanobacterial cells by neutron spectroscopy

  • Neutron data were collected at 20 °C during 12-hour light and dark alternating cycles to mimic the circadian clock

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Summary

OPEN Revealing the Dynamics of Thylakoid Membranes in Living

Laura-Roxana Stingaciu[1], Hugh O’Neill[2], Michelle Liberton[3], Volker S. Neutron Spin-Echo[13] (NSE) is a high-resolution spectroscopic technique that has already proved to be a successful method of studying the structure and dynamics of model bilayer lipid membranes[14,15,16,17] and proteins in solution[18] but has far not been used to study the internal dynamics of intact living cell components This technique allows simultaneous observation of correlation times and length scales and thereby can directly deduce the geometry and modes of motion observed, such as membrane undulation or diffusion, which are not possible using purely energy-resolved spectroscopic techniques

We used the NSE spectrometer at the Spallation
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