Spatially segregated transcription and translation in cells of the endomembrane-containing bacterium Gemmata obscuriglobus

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 30; pp. 11067 - 11072
• Main Authors: Gottshall, Ekaterina Y., Seebart, Corrine, Gatlin, Jesse C., Ward, Naomi L.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 29.07.2014; National Acad Sciences
• Subjects: Animal cells; Antibodies; Bacillus subtilis; Bacteria; Bacterial Proteins - biosynthesis; Bacterial Proteins - genetics; Biological Sciences; Cell Membrane - genetics; Cell Membrane - metabolism; Cell separation; Cells; DNA; Escherichia coli; Eukaryotes; Evolution; Gemmata obscuriglobus; Gene expression; Gene Expression Regulation, Bacterial - physiology; Messenger RNA; Microscopy; Morphology; Nuclear membrane; Phylogenetics; Planctomycetales - classification; Planctomycetales - genetics; Planctomycetales - metabolism; Protein Biosynthesis - physiology; Ribosomes; Transcription, Genetic - physiology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1409187111

The dogma of coupled transcription and translation in bacteria has been challenged by recent reports of spatial segregation of these processes within the relatively simple cellular organization of the model organisms Escherichia coli and Bacillus subtilis . The bacterial species Gemmata obscuriglobus possesses an extensive endomembrane system. The membranes generate a very convoluted intracellular architecture in which some of the cell’s ribosomes appear to have less direct access to the cell’s nucleoid(s) than others. This observation prompted us to test the hypothesis that a substantial proportion of G. obscuriglobus translation may be spatially segregated from transcription. Using immunofluorescence and immunoelectron microscopy, we showed that translating ribosomes are localized throughout the cell, with a quantitatively greater proportion found in regions distal to nucleoid(s). Our results extend information about the phylogenetic and morphological diversity of bacteria in which the spatial organization of transcription and translation has been studied. These findings also suggest that endomembranes may provide an obstacle to colocated transcription and translation, a role for endomembranes that has not been reported previously for a prokaryotic organism. Our studies of G. obscuriglobus may provide a useful background for consideration of the evolutionary development of eukaryotic cellular complexity and how it led to decoupled processes of gene expression in eukaryotes.