Three-dimensional ultrastructure of a unicellular cyanobacterium.

Abstract

The first complete three-dimensional ultrastructural reconstruction of a cyanobacterium was accomplished with high-voltage electron microscopy and computer-aided assembly of serial sections. The precise arrangement of subcellular features within the cell body was very consistent from one cell to another. Specialized inclusion bodies always occupied specific intracellular locations. The photosynthetic thylakoid membranes entirely surrounded the central portion of the cytoplasm, thereby compartmentalizing it from the rest of the cell. The thylakoid membranes formed an interconnecting network of concentric shells, merging only at the inner surface of the cytoplasmic membrane. The thylakoids were in contact with the cytoplasmic membrane at several locations, apparently to maintain the overall configuration of the thylakoid system. These results clarified several unresolved issues regarding structurefunction relationships in cyanobacteria.Cyanobacteria (blue-green algae) are phototrophic microorganisms that carry out a form of oxygenic photosynthesis similar to that of green plants. The internal organization of the cyanobacterial cell is prokaryotic, yet these organisms are considerably more structurally complicated than most other types of bacteria. The ultrastructure ofcyanobacteria has been studied extensively, and much is known about their basic subeellular features, the structural differences among the various genera and groups, and the effects of environmental factors on internal structures. (For reviews, see references 1-3.) Little is known, however, about how the ultrastructural features of cyanobacteria are arranged three-dimensionally within the cell. Most speculations concerning the three-dimensional architecture of these organisms have come about through extrapolation of the information in randomly cut, individual thin sections. There have been no reports describing three-dimensional reconstructions of entire cyanobacterial cells by serial sectioning or any other approach. Reconstructions of this type are needed, however, because they (a) would eliminate the need for extrapolation, (b) can resolve a number of uncertain issues in regard to cyanobacterial ultrastructure (see below), and (c) may lead to a better understanding of structure-function relationships in the cyanobacterial cell.Complete three-dimensional reconstructions of whole cells or cell organelles have been relatively rare because, until recently, the techniques for completing such reconstructions were cumbersome and time-consuming. However, the application of high-voltage electron microscopy (HVEM ~) to biological materials has now made it possible to view serial thick (0.25-1.0 tzm) sections without any significant loss in resolution (4-7). Since these sections are much thicker than conventional thin sections, fewer of them are required to cover a given sample volume during serial sectioning. Three-dimensional reconstructions have also been greatly facilitated by the development of computer programs designed to collect the informat...

Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

“…It was suggested that, during the transition of proplastids to chloroplasts, thylakoid membranes originate from invaginations of the inner envelope in algal chloroplasts or proplastids of vascular plants, while in mature chloroplasts, the membrane system is maintained by vesicle transport (Rast et al, 2015). Contact points of thylakoid membranes with the plasma membrane were seen in 3D micrographs of a cyanobacterium (Nierzwicki-Bauer et al, 1983). Evidence to support this model in higher plants has been challenging due to the transient nature of membrane remodeling in plastids (Shimoni et al, 2005).…”

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

“…Explorations of the ultrastructure of cyanobacterial cells in three dimensions began with computer-aided reconstructions of serial sections of Synechococcus sp. PCC 7002 (formerly Agmenellum quadruplicatum; Nierzwicki-Bauer et al, 1983), and progressed to using advanced techniques such as electron tomography and cryo-electron tomography. Recent analyses of tomographic data collected from #200-nm-thick sections through cyanobacterial cells have shown that thylakoid membranes are connected by junctions and channels linking adjacent membranes in Prochlorococcus strains MIT9313 and MED4 (Ting et al, 2007) and by branching and fusion in Microcoleus sp.…”

Deletion of Synechocystis sp. PCC 6803 Leader Peptidase LepB1 Affects Photosynthetic Complexes and Respiration

“…The ultrastructure and organization of the membranes is however still under debate and mainly two different opinions prevail concerning the organization of plasma and thylakoid membranes. One is that the two membranes are continuous, making the periplasm and lumen a common compartment, the second that the membranes are completely separated (1)(2)(3)(4)(5)(6)(7)(8)(9).…”

“…Knockout mutations of the two genes, however, give significantly different results: whereas LepB2 appears to be totally essential for cell viability, cells with a deletion in LepB1 are still able to grow under heterotrophic conditions in dim light (26). The light sensitivity disappeared when 3-(3,4-dichlorophenyl)-1,1-dimetylurea (DCMU) 1 was present. DCMU inhibits the reduction of the plastoquinone (PQ) pool by photosystem II (PSII) and this indicates that the primary cause for the photosensitivity observed is the impairment in electron flow downstream of PSII.…”