title: Conserved Units of Co-Expression in Bacterial Genomes: An Evolutionary Insight into Transcriptional Regulation.
abstract: Genome-wide measurements of transcriptional activity in bacteria indicate that the transcription of successive genes is strongly correlated beyond the scale of operons. Here, we analyze hundreds of bacterial genomes to identify supra-operonic segments of genes that are proximal in a large number of genomes. We show that these synteny segments correspond to genomic units of strong transcriptional co-expression. Structurally, the segments contain operons with specific relative orientations (co-directional or divergent) and nucleoid-associated proteins are found to bind at their boundaries. Functionally, operons inside a same segment are highly co-expressed even in the apparent absence of regulatory factors at their promoter regions. Remote operons along DNA can also be co-expressed if their corresponding segments share a transcriptional or sigma factor, without requiring these factors to bind directly to the promoters of the operons. As evidence that these results apply across the bacterial kingdom, we demonstrate them both in the Gram-negative bacterium Escherichia coli and in the Gram-positive bacterium Bacillus subtilis. The underlying process that we propose involves only RNA-polymerases and DNA: it implies that the transcription of an operon mechanically enhances the transcription of adjacent operons. In support of a primary role of this regulation by facilitated co-transcription, we show that the transcription en bloc of successive operons as a result of transcriptional read-through is strongly and specifically enhanced in synteny segments. Finally, our analysis indicates that facilitated co-transcription may be evolutionary primitive and may apply beyond bacteria.
authors.affiliation: CNRS, TIMC-IMAG, F-38000 Grenoble, France.|Univ. Grenoble Alpes, TIMC-IMAG, F-38000 Grenoble, France.
authors.forename: Ivan
authors.initials: I
authors.lastname: Junier
authors.affiliation: CNRS, LIPhy, F-38000 Grenoble, France.|Univ. Grenoble Alpes, LIPhy, F-38000 Grenoble, France.
authors.forename: Olivier
authors.initials: O
authors.lastname: Rivoire
mesh_terms: D001412:Bacillus subtilis / Q000235:genetics; D001665:Binding Sites; D004269:DNA, Bacterial / Q000235:genetics*; D012321:DNA-Directed RNA Polymerases / Q000235:genetics; D030541:Databases, Genetic; D004926:Escherichia coli / Q000235:genetics; D019143:Evolution, Molecular; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D016680:Genome, Bacterial; D020411:Oligonucleotide Array Sequence Analysis; D009876:Operon; D011401:Promoter Regions, Genetic; D012808:Sigma Factor / Q000235:genetics; D013269:Stochastic Processes; D026801:Synteny; D014158:Transcription, Genetic
chemical_list: D004269:DNA, Bacterial; D012808:Sigma Factor; D012321:DNA-Directed RNA Polymerases