Dynamics of translation can determine the spatial organization of membrane-bound proteins and their mRNA

Significance Unlike their eukaryotic counterparts, bacterial cells are composed of a single compartment. This allows many rapidly diffusing macromolecules, such as proteins and mRNAs, to be evenly distributed in the cell. Important exceptions are proteins embedded in the cell membrane, which transport material and information across the membrane. Often these proteins attach to the membrane before their translation is complete, anchoring their mRNAs to the vicinity of the membrane. This coupling between translation and localization suggests that the dynamics of translation may shape the spatial organization. In this paper, we use a canonical model of nonequilibrium statistical physics to characterize this connection and show how tunable kinetic properties allow the cell to regulate the spatial organization of both mRNAs and proteins. Unlike most macromolecules that are homogeneously distributed in the bacterial cell, mRNAs that encode inner-membrane proteins can be concentrated near the inner membrane. Cotranslational insertion of the nascent peptide into the membrane brings the translating ribosome and the mRNA close to the membrane. This suggests that kinetic properties of translation can determine the spatial organization of these mRNAs and proteins, which can be modulated through posttranscriptional regulation. Here we use a simple stochastic model of translation to characterize the effect of mRNA properties on the dynamics and statistics of its spatial distribution. We show that a combination of the rate of translation initiation, the availability of secretory apparatuses, and the composition of the coding region determines the abundance of mRNAs near the membrane, as well as their residence time. We propose that the spatiotemporal dynamics of mRNAs can give rise to protein clusters on the membrane and determine their size distribution.