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Aging and death in an organism that reproduces by morphologically symmetric division - PubMed

Aging and death in an organism that reproduces by morphologically symmetric division

Eric J Stewart et al. PLoS Biol. 2005 Feb.

Abstract

In macroscopic organisms, aging is often obvious; in single-celled organisms, where there is the greatest potential to identify the molecular mechanisms involved, identifying and quantifying aging is harder. The primary results in this area have come from organisms that share the traits of a visibly asymmetric division and an identifiable juvenile phase. As reproductive aging must require a differential distribution of aged and young components between parent and offspring, it has been postulated that organisms without these traits do not age, thus exhibiting functional immortality. Through automated time-lapse microscopy, we followed repeated cycles of reproduction by individual cells of the model organism Escherichia coli, which reproduces without a juvenile phase and with an apparently symmetric division. We show that the cell that inherits the old pole exhibits a diminished growth rate, decreased offspring production, and an increased incidence of death. We conclude that the two supposedly identical cells produced during cell division are functionally asymmetric; the old pole cell should be considered an aging parent repeatedly producing rejuvenated offspring. These results suggest that no life strategy is immune to the effects of aging, and therefore immortality may be either too costly or mechanistically impossible in natural organisms.

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Figures

Figure 1
Figure 1. The Life Cycle of E. coli

During cell division, two new poles are formed, one in each of the progeny cells (new poles, shown in blue). The other ends of those cells were formed during a previous division (old poles, shown in red). (A) The number of divisions since each pole was formed is indicated by the number inside the pole. Using the number of divisions since the older pole of each cell was formed, it is possible to assign an age in divisions to that cell, as indicated. Similarly, cells that consecutively divided as a new pole are assigned a new pole age, based on the current, consecutive divisions as a new pole cell. (B) Time-lapse images of growing cells corresponding to the stages in (A). False color has been added to identify the poles.

Figure 2
Figure 2. Average Lineage Showing Old Pole Effect on Growth Rate

The first division in the microcolonies is not represented, as the identity of the poles is not known until after one division (hence each initial cell gives rise to two lineages that are tracked separately, and subsequently combined from all films to create the single average lineage shown here). The lengths of the lines connecting cells to their progeny are proportional to the average growth rate of that cell; a longer line represents a higher growth rate for that cell. At each division, the cell inheriting the old pole is placed on the right side of the division pair, and shown in red, while new poles are placed on the left side of each pair, and shown in blue (note that this choice of orientation is not the same as that of Figure 1, to compare more easily old and new pole lineages). Because the position of the start of the growth line for each new generation is dependent on the generations that preceded it, the difference in growth rates is cumulative. Green lines indicate the point at which the first cell divides in the last four generations. Nine generations from 94 films encompassing 35,049 cells are included in this tree. The average growth rate of all the cells corresponds to a doubling time of 28.2+/−0.1 min. The data used to generate the average lineage are provided in Dataset S1.

Figure 3
Figure 3. The Effects of Consecutive Divisions as an Old or New Pole on Growth Rate

(A) The cellular growth rate, represented on the y-axis, is normalized to the growth rate of all cells from the same generation and geography in each film. On the x-axis consecutive divisions are seen as either a new pole (open circles), showing rejuvenation, or an old pole (closed circles), showing aging. Cells represented at each point: new pole divisions 1–7: 7,730; 3,911; 1,956; 984; 465; 211; 89; old pole divisions 1–7: 4,687; 3,833; 1,933; 956; 465; 213; 75. (B) Pair comparison of the growth rates of sibling cells. The division age of the old pole sibling (the mother cell) is shown on the x-axis. The percentage difference between the growth rate of the new pole sibling (the daughter cell) and this cell is shown on the y-axis. A positive difference corresponds to a faster growth rate for the new pole cell. Cell pairs represented at each point, ages 1–7: 9,722; 4,824; 2,409; 1,202; 601; 282; 127. In both graphs, cells are from all 94 films. The error bars represent the standard error of the mean. The old and new pole growth rates in (A) and the pair differences in (B) are fitted to a line to show the trend; however, the actual progressions may not be linear (R 2 old poles = 0.97, new poles = 0.83, pair difference = 0.94).

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References

    1. Kirkwood TBL, Holliday R. The evolution of ageing and longevity. Proc R Soc Lond B Biol Sci. 1979;205:531–546. - PubMed
    1. Partridge L, Barton NH. Optimality, mutation and the evolution of ageing. Nature. 1993;362:305–311. - PubMed
    1. Ackermann M, Stearns SC, Jenal U. Senescence in a bacterium with asymmetric division. Science. 2003;300:1920. - PubMed
    1. Nystrom T. Aging in bacteria. Curr Opin Microbiol. 2002;5:596–601. - PubMed
    1. Sinclair DA. Paradigms and pitfalls of yeast longevity research. Mech Ageing Dev. 2002;123:857–867. - PubMed

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