Spatial organization of the flow of genetic information in bacteria.
Eukaryotic cells spatially organize mRNA processes such as translation and mRNA decay. Much less is clear in bacterial cells where the spatial distribution of mature mRNA remains ambiguous. Using a sensitive method based on quantitative fluorescence in situ hybridization, we show here that in Caulobacter crescentus and Escherichia coli, chromosomally expressed mRNAs largely display limited dispersion from their site of transcription during their lifetime. We estimate apparent diffusion coefficients at least two orders of magnitude lower than expected for freely diffusing mRNA, and provide evidence in C. crescentus that this mRNA localization restricts ribosomal mobility. Furthermore, C. crescentus RNase E appears associated with the DNA independently of its mRNA substrates. Collectively, our findings show that bacteria can spatially organize translation and, potentially, mRNA decay by using the chromosome layout as a template. This chromosome-centric organization has important implications for cellular physiology and for our understanding of gene expression in bacteria.
Montero Llopis
Paula
P
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA.
Jackson
Audrey F
AF
Sliusarenko
Oleksii
O
Surovtsev
Ivan
I
Heinritz
Jennifer
J
Emonet
Thierry
T
Jacobs-Wagner
Christine
C
D001426:Bacterial Proteins / Q000235:genetics; D016935:Caulobacter crescentus / Q000166:cytology / Q000235:genetics* / Q000378:metabolism*; D018833:Chaperonins / Q000235:genetics; D002876:Chromosomes, Bacterial / Q000235:genetics / Q000378:metabolism; D004269:DNA, Bacterial / Q000378:metabolism; D004058:Diffusion; D004722:Endoribonucleases / Q000378:metabolism; D004926:Escherichia coli / Q000166:cytology / Q000235:genetics* / Q000378:metabolism*; D015964:Gene Expression Regulation, Bacterial; D017404:In Situ Hybridization, Fluorescence; D007763:Lac Operon / Q000235:genetics; D014176:Protein Biosynthesis; D020871:RNA Stability; D034443:RNA Transport; D012329:RNA, Bacterial / Q000032:analysis / Q000235:genetics / Q000378:metabolism*; D012333:RNA, Messenger / Q000032:analysis / Q000235:genetics / Q000378:metabolism; D012270:Ribosomes / Q000378:metabolism; D014158:Transcription, Genetic / Q000235:genetics
D001426:Bacterial Proteins; D004269:DNA, Bacterial; C097970:GroESL protein, Bacteria; D012329:RNA, Bacterial; D012333:RNA, Messenger; D004722:Endoribonucleases; C022537:ribonuclease E; D018833:Chaperonins