Allocation of gene products to daughter cells is determined by the age of the mother in single Escherichia coli cells.

Gene expression and growth rate are highly stochastic in Escherichia coli. Some of the growth rate variations result from the deterministic and asymmetric partitioning of damage by the mother to its daughters. One daughter, denoted the old daughter, receives more damage, grows more slowly and ages. To determine if expressed gene products are also allocated asymmetrically, we compared the levels of expressed green fluorescence protein in growing daughters descending from the same mother. Our results show that old daughters were less fluorescent than new daughters. Moreover, old mothers, which were born as old daughters, produced daughters that were more asymmetric when compared to new mothers. Thus, variation in gene products in a clonal E. coli population also has a deterministic component. Because fluorescence levels and growth rates were positively correlated, the aging of old daughters appears to result from both the presence of both more damage and fewer expressed gene products.

Asymmetrical Damage Partitioning in Bacteria: A Model for the Evolution of Stochasticity, Determinism, and Genetic Assimilation.

Non-genetic phenotypic variation is common in biological organisms. The variation is potentially beneficial if the environment is changing. If the benefit is large, selection can favor the evolution of genetic assimilation, the process by which the expression of a trait is transferred from environmental to genetic control. Genetic assimilation is an important evolutionary transition, but it is poorly understood because the fitness costs and benefits of variation are often unknown. Here we show that the partitioning of damage by a mother bacterium to its two daughters can evolve through genetic assimilation. Bacterial phenotypes are also highly variable. Because gene-regulating elements can have low copy numbers, the variation is attributed to stochastic sampling. Extant Escherichia coli partition asymmetrically and deterministically more damage to the old daughter, the one receiving the mother's old pole. By modeling in silico damage partitioning in a population, we show that deterministic asymmetry is advantageous because it increases fitness variance and hence the efficiency of natural selection. However, we find that symmetrical but stochastic partitioning can be similarly beneficial. To examine why bacteria evolved deterministic asymmetry, we modeled the effect of damage anchored to the mother's old pole. While anchored damage strengthens selection for asymmetry by creating additional fitness variance, it has the opposite effect on symmetry. The difference results because anchored damage reinforces the polarization of partitioning in asymmetric bacteria. In symmetric bacteria, it dilutes the polarization. Thus, stochasticity alone may have protected early bacteria from damage, but deterministic asymmetry has evolved to be equally important in extant bacteria. We estimate that 47% of damage partitioning is deterministic in E. coli. We suggest that the evolution of deterministic asymmetry from stochasticity offers an example of Waddington's genetic assimilation. Our model is able to quantify the evolution of the assimilation because it characterizes the fitness consequences of variation.