Abstract
Cyanobacteria are prokaryotes that can use photosynthesis to convert sunlight into cellular fuel. Knowledge of the organization of the membrane systems in cyanobacteria is critical to understanding the metabolic processes in these organisms. We examined the wild-type strain of Synechocystis sp. PCC 6803 and a series of mutants with altered light-harvesting phycobilisome antenna systems for changes in thylakoid membrane architecture under different conditions. Using small-angle neutron scattering, it was possible to resolve correlation distances of subcellular structures in live cells on the nanometer scale and capture dynamic light-induced changes to these distances. Measurements made from samples with varied scattering contrasts confirmed that these distances could be attributed to the thylakoid lamellar system. We found that the changes to the thylakoid system were reversible between light- and dark-adapted states, demonstrating a robust structural flexibility in the architecture of cyanobacterial cells. Chemical disruption of photosynthetic electron transfer diminished these changes, confirming the involvement of the photosynthetic apparatus. We have correlated these findings with electron microscopy data to understand the origin of the changes in the membranes and found that light induces an expansion in the center-to-center distances between the thylakoid membrane layers. These combined data lend a dynamic dimension to the intracellular organization in cyanobacterial cells.
Highlights
In cyanobacteria, light harvesting and photosynthesis occur in the thylakoid membranes
Cyanobacteria such as Synechocystis 6803 have a highly organized thylakoid membrane architecture, and it has been proposed that rearrangements in the membrane system and the spacing between membrane layers play a role in the cellular regulation of photosynthesis [10]
The length scales of interest in this context range from the thickness of individual lipid bilayers to the spacing between thylakoid membrane layers, which are covered by small-angle scattering techniques using x-rays or neutrons (SANS)
Summary
Light harvesting and photosynthesis occur in the thylakoid membranes. SANS can be used to characterize periodically organized biological membrane systems on smaller length scales by observing diffraction from regularly spaced structural features separated by ϳ1–200 nm [11] Both the accessible length scales and the ability to examine individual components of biological systems using contrast matching have led to the application of SANS in studies of cyanobacteria, eukaryotic algae, plant thylakoids [8, 12], and mammalian mitochondria [13]. To examine thylakoid membrane organization in cyanobacterial cells under different conditions, we used a correlative approach incorporating both transmission electron microscopy (TEM) and SANS These techniques both provide complementary data at the length scales relevant to the study of biological structures, including membranes. Our data indicate that the photosynthetic membranes in Synechocystis 6803 have a structural plasticity that is tied to the function of the photosynthetic electron transfer chain
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