Efficiency and Robustness to Nonoptimal Temperatures of Nucleoid Exclusion Processes in Escherichia coli

In Escherichia coli, the functioning of various cellular processes depends on the internal spatial organization of the cell. One of the agents for this cellular organization is the nucleoid, whose density, higher than the cytoplasm’s, is responsible for the segregation and retention of macromolecules, such as protein aggregates and chemotaxis complexes, at the cell poles and the placement of the Z-ring at midcell. For the cell to thrive in fluctuating environments, these processes — the segregation of protein aggregates, the polarization of the chemotaxis network and the Z-ring positioning — need to be efficient in optimal conditions, but also robust to suboptimal conditions. We studied the efficiency of the positioning of Z-rings, chemotaxis networks, and protein aggregates, as a function of the nucleoid(s) morphology and temperature. We show that their spatial distributions along the major cell axis are indirectly influenced by temperature, in agreement with the nucleoid(s) morphology and its volume-exclusion phenomenon in each temperature condition. In particular, we find that temperature changes, by altering the nucleoid size, cause changes in how efficiently the cell is able to contain these three cellular components in a particular region of the cell. This is most visible in the observed linear correlation between the Kurtosis of the spatial distributions of these cellular components along the major cell axis and the spatial properties of the nucleoid(s) (nucleoid size for protein aggregates and Tsr clusters and distance between nucleoids prior to cell division for Z-rings). Finally, it was also found a negative linear correlation between the efficiency of the three processes at optimal temperatures and their robustness to suboptimal temperatures. Overall, these results suggest that the robustness of the biophysical properties of the nucleoid to temperature shifts are of importance to the ability of E. coli to thrive in non-optimal temperatures.