Spatial and genetic constraints govern transcription–translation coupling and mRNA degradation in bacteria

Bacterial gene expression is thought to involve tightly coupled transcription, translation and mRNA degradation. However, recent work has indicated that this is not always the case, leaving the generality and regulation of this coordination unclear. Here we use genetic, kinetic and spatial analyses in Escherichia coli to show that transcription–translation coupling requires high translational activity and that nearly half of the transcriptome exhibits signatures consistent with partial uncoupling. We find that co-transcriptional mRNA degradation is rare due to membrane localization of RNase E, except for transcripts encoding inner-membrane proteins. Our results show that translation efficiency determines the level of premature transcription termination, which in turn shapes mRNA degradation patterns and kinetics. Comparative analyses in Bacillus subtilis and Caulobacter crescentus also reveal species-specific coordination strategies. This challenges the universality of co-transcriptional coupling and defines how spatial and genetic features coordinate bacterial gene expression. RNase E localization and translation initiation coordinate transcription, translation and mRNA degradation during the life cycle of an mRNA, explaining gene- and species-specific variations in this coordination in bacteria.