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.
Highlights
Cyanobacteria, descendants of the endosymbiont that gave rise to modern-day chloroplasts, are vital contributors to global biological energy conversion processes
By using serial electron tomography combined with montaging, we were able to reconstruct large volumes of cyanobacterial cells in three dimensions, to our knowledge the first report of such extensive reconstructions in an oxygenic photosynthetic prokaryote
Cyanobacteria related to Cyanothece 51142 have recently been recognized for their contributions to nitrogen fixation in the open oceans (Zehr et al, 2001)
Summary
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. 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. In a number of strains of cyanobacteria, thylakoid membranes appear to follow the shape of the cell envelope, forming multiple concentric membrane layers interior to the plasma membrane (Mullineaux, 1999) This type of organization is evident in widely studied strains such as Synechocystis sp. The extensive nature of the thylakoid membrane network and the intricate detail of its organization were not apparent in random thin-section electron micrographs, or even in small-volume tomograms, but were readily observable in the larger-volume tomographic data presented here
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