Dataset Information

Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria.

ABSTRACT: Cyanobacteria, the progenitors of plant and algal chloroplasts, enabled aerobic life on earth by introducing oxygenic photosynthesis. In most cyanobacteria, the photosynthetic membranes are arranged in multiple, seemingly disconnected, concentric shells. In such an arrangement, it is unclear how intracellular trafficking proceeds and how different layers of the photosynthetic membranes communicate with each other to maintain photosynthetic homeostasis. Using electron microscope tomography, we show that the photosynthetic membranes of two distantly related cyanobacterial species contain multiple perforations. These perforations, which are filled with particles of different sizes including ribosomes, glycogen granules and lipid bodies, allow for traffic throughout the cell. In addition, different layers of the photosynthetic membranes are joined together by internal bridges formed by branching and fusion of the membranes. The result is a highly connected network, similar to that of higher-plant chloroplasts, allowing water-soluble and lipid-soluble molecules to diffuse through the entire membrane network. Notably, we observed intracellular membrane-bounded vesicles, which were frequently fused to the photosynthetic membranes and may play a role in transport to these membranes.

SUBMITTER: Nevo R

PROVIDER: S-EPMC1817639 | biostudies-literature | 2007 Mar

REPOSITORIES: biostudies-literature

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Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria.

Nevo Reinat R Charuvi Dana D Shimoni Eyal E Schwarz Rakefet R Kaplan Aaron A Ohad Itzhak I Reich Ziv Z

The EMBO journal 20070215 5

Cyanobacteria, the progenitors of plant and algal chloroplasts, enabled aerobic life on earth by introducing oxygenic photosynthesis. In most cyanobacteria, the photosynthetic membranes are arranged in multiple, seemingly disconnected, concentric shells. In such an arrangement, it is unclear how intracellular trafficking proceeds and how different layers of the photosynthetic membranes communicate with each other to maintain photosynthetic homeostasis. Using electron microscope tomography, we sh ...[more]

PMID: 17304210

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Project description:While photosynthetic processes have become increasingly understood in cyanobacterial model strains, differences in the spatial distribution of thylakoid membranes among various lineages have been largely unexplored. Cyanobacterial cells exhibit an intriguing diversity in thylakoid arrangements, ranging from simple parietal to radial, coiled, parallel, and special types. Although metabolic background of their variability remains unknown, it has been suggested that thylakoid patterns are stable in certain phylogenetic clades. For decades, thylakoid arrangements have been used in cyanobacterial classification as one of the crucial characters for definition of taxa. The last comprehensive study addressing their evolutionary history in cyanobacteria was published 15 years ago. Since then both DNA sequence and electron microscopy data have grown rapidly. In the current study, we map ultrastructural data of >200 strains onto the SSU rRNA gene tree, and the resulting phylogeny is compared to a phylogenomic tree. Changes in thylakoid architecture in general follow the phylogeny of housekeeping loci. Parietal arrangement is resolved as the original thylakoid organization, evolving into complex arrangement in the most derived group of heterocytous cyanobacteria. Cyanobacteria occupying intermediate phylogenetic positions (greater filamentous, coccoid, and baeocytous types) exhibit fascicular, radial, and parallel arrangements, partly tracing the reconstructed course of phylogenetic branching. Contrary to previous studies, taxonomic value of thylakoid morphology seems very limited. Only special cases such as thylakoid absence or the parallel arrangement could be used as taxonomically informative apomorphies. The phylogenetic trees provide evidence of both paraphyly and reversion from more derived architectures in the simple parietal thylakoid pattern. Repeated convergent evolution is suggested for the radial and fascicular architectures. Moreover, thylakoid arrangement is constrained by cell size, excluding the occurrence of complex architectures in cyanobacteria smaller than 2 μm in width. It may further be dependent on unknown (eco)physiological factors as suggested by recurrence of the radial type in unrelated but morphologically similar cyanobacteria, and occurrence of special features throughout the phylogeny. No straightforward phylogenetic congruences have been found between proteins involved in photosynthesis and thylakoid formation, and the thylakoid patterns. Remarkably, several postulated thylakoid biogenesis factors are partly or completely missing in cyanobacteria, challenging their proposed essential roles.

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Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria.

Publications

Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria.

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