Spatial and temporal distribution of ribosomes in single cells reveals aging differences between old and new daughters of Escherichia coli

Abstract

Lineages of rod-shaped bacteria such as Escherichia coli exhibit a temporal decline in elongation rate in a manner comparable to cellular or biological aging. The effect results from the production of asymmetrical daughters, one with a lower elongation rate, by the division of a mother cell. The slower daughter compared to the faster daughter, denoted respectively as the old and new daughters, has more aggregates of damaged proteins and fewer expressed gene products. We have examined further the degree of asymmetry by measuring the density of ribosomes between old and new daughters and between their poles. We found that ribosomes were denser in the new daughter and also in the new pole of the daughters. These ribosome patterns match the ones we previously found for expressed gene products. This outcome suggests that the asymmetry is not likely to result from properties unique to the gene expressed in our previous study, but rather from a more fundamental upstream process affecting distribution of ribosomal abundance. Because damage aggregates and ribosomes are both more abundant at the poles of E. coli cells, we suggest that competition for space between the two could explain the reduced ribosomal density in old daughters. Using published values for aggregate sizes and the relationship between ribosomal number and elongation rates, we show that the aggregate volumes could in principle displace quantitatively the amount of ribosomes needed to reduce the elongation rate of the old daughters. IMPORTANCEBacteria exhibit a growth decline in a manner comparable to cellular or biological aging. When a mother bacterium reproduces by binary fission it allocates more damage to one of the two daughters. The extra damage correlates with a slower growth. Thus, a lineage of daughters successively acquiring more damage over generations ages, sometimes even to death under stressful conditions. Aging lineages also have lower levels of expressed gene products. Here we show that the aging process also correlates with lower cellular levels of ribosomes. The identification of a ribosomal effect shows that the aging process is acting at a much more fundamental upstream level. While decreased gene products could have resulted from local regulation of specific genes, a lower ribosomal density affects the entirety of cellular metabolism. Understanding bacterial aging is important because biological aging may have originated in single-celled organisms such as E. coli.