Unique Thylakoid Membrane Architecture of a Unicellular N2-Fixing Cyanobacterium Revealed by Electron Tomography    

Abstract

Cyanobacteria, descendants of the endosymbiont that gave rise to modern-day chloroplasts, are vital contributors to global biological energy conversion processes. A thorough understanding of the physiology of cyanobacteria requires detailed knowledge of these organisms at the level of cellular architecture and organization. In these prokaryotes, the large membrane protein complexes of the photosynthetic and respiratory electron transport chains function in the intracellular thylakoid membranes. Like plants, the architecture of the thylakoid membranes in cyanobacteria has direct impact on cellular bioenergetics, protein transport, and molecular trafficking. However, whole-cell thylakoid organization in cyanobacteria is not well understood. Here we present, by using electron tomography, an in-depth analysis of the architecture of the thylakoid membranes in a unicellular cyanobacterium, Cyanothece sp. ATCC 51142. Based on the results of three-dimensional tomographic reconstructions of near-entire cells, we determined that the thylakoids in Cyanothece 51142 form a dense and complex network that extends throughout the entire cell. This thylakoid membrane network is formed from the branching and splitting of membranes and encloses a single lumenal space. The entire thylakoid network spirals as a peripheral ring of membranes around the cell, an organization that has not previously been described in a cyanobacterium. Within the thylakoid membrane network are areas of quasi-helical arrangement with similarities to the thylakoid membrane system in chloroplasts. This cyanobacterial thylakoid arrangement is an efficient means of packing a large volume of membranes in the cell while optimizing intracellular transport and trafficking.

Photosynthetic Pigment Localization and Thylakoid Membrane Morphology Are Altered in Synechocystis 6803 Phycobilisome Mutants

“…Cells were prepared for electron microscopy essentially as described (Liberton et al, 2011). Culture aliquots (approximately 15 mL) were centrifuged, and the pellet was resuspended in a small volume, transferred to planchettes with 100-to 200-mm-deep wells, and frozen in a Baltec High Pressure Freezer (Bal-Tec).…”

Global Proteomic Analysis Reveals an Exclusive Role of Thylakoid Membranes in Bioenergetics of a Model Cyanobacterium

“…PCC 6803 convert light to cellular energy, an ability that makes these organisms of particular interest in renewable energy studies. Cyanobacteria typically have a Gram-negative-type cell envelope consisting of a plasma membrane (PM) 1 , peptidoglycan layer, and outer membrane. These microbes also have an internal thylakoid membrane (TM) system where the protein complexes of the photosynthetic and respiratory electron transfer chains function.…”

Insights into the complex 3-D architecture of thylakoid membranes in unicellular cyanobacterium Cyanothece sp. ATCC 51142

“…This architecture is similar to what we reported in our examination of cells from the L10 time point. 13 In tomographic slice images, the thylakoid membranes appeared sheet-like and the areas where the membranes branched could be clearly observed (Fig. 1A-E).…”

“…In fact, only within the past few years has work using tomographic data shown that thylakoid membranes are connected by channels or bridging membranes in some cyanobacterial strains. 11,12 Our recent work 13 examining the thylakoid membrane system in Cyanothece 51142 depicted, for the first time, a membrane system in a cyanobacterium with strong similarities to that in plants: a highly interconnected network composed by branching is very dense, with a larger number of membrane layers compared to what has been observed in other cyanobacteria. 13 It is possible that helical organization originated as a primarily left-handed architecture, followed by the development of grana and the attendant right-handedness of the grana-stroma architecture at a later time.…”

“…11,12 Our recent work 13 examining the thylakoid membrane system in Cyanothece 51142 depicted, for the first time, a membrane system in a cyanobacterium with strong similarities to that in plants: a highly interconnected network composed by branching is very dense, with a larger number of membrane layers compared to what has been observed in other cyanobacteria. 13 It is possible that helical organization originated as a primarily left-handed architecture, followed by the development of grana and the attendant right-handedness of the grana-stroma architecture at a later time. It is tempting to speculate, particularly in light of the recent analysis of stroma thylakoids, 10 that the chloroplast stroma thylakoid arrangement and the thylakoid architecture in Cyanothece 51142 can be compared directly, with the addition green and yellow membrane regions, respectively, in Fig.…”