Temporal Dynamics of Bacterial Aging and Rejuvenation

Abstract

Single-celled organisms dividing by binary fission were thought not to age [1-4]. A 2005 study by Stewart et al. [5] reversed the dogma by demonstrating that Escherichia coli were susceptible to aging. A follow-up study by Wang et al. [6] countered those results by demonstrating that E. coli cells trapped in microfluidic devices are able to sustain robust growth without aging. The present study reanalyzed these conflicting data by applying a population genetic model for aging in bacteria [7]. Our reanalysis showed that in E. coli, as predicted by the model, (1) aging and rejuvenation occurred simultaneously in a population; (2) lineages receiving sequentially the maternal old pole converged to a stable attractor state; (3) lineages receiving sequentially the maternal new pole converged to an equivalent but separate attractor state; (4) cells at the old pole attractor had a longer doubling time than ones at the new pole attractor; and (5) the robust growth state identified by Wang et al. corresponds to our predicted attractor for lineages harboring the maternal old pole. Thus, the previous data, rather than opposing each other, together provide strong evidence for bacterial aging.

Ageing in Escherichia coli requires damage by an extrinsic agent

“…A second study soon countered those results by showing that E. coli cells trapped in micro-fluidic devices sustained robust growth with no lineage ageing (Wang et al, 2010). By reinterpreting the data of Stewart and colleagues and Wang and colleagues from the perspective of a population genetic model, we were able to reconcile the differences and show that both studies together provided strong support for lineage ageing in E. coli (Rang et al, 2011). However, a more recent paper that tested for lineage ageing in E. coli under high and low glucose concentrations again reported no asymmetry between the growth rates of daughters (Lele et al, 2011).…”

“…The model has been used successfully to estimate the mean and confidence intervals of these three parameters (Chao, 2010). It has also been used to make testable predictions (Rang et al, 2011) that reconcile the differences between the results of Stewart et al (2005) and Wang et al (2010). The parameters a and l are key for the present study because they quantify the hypothesized effect of streptomycin on bacterial ageing.…”

“…Why then did Stewart and colleagues and some of the recent studies succeed in finding bacterial ageing (Lindner et al, 2008;Rang et al, 2011;Stewart et al, 2005;Veening et al, 2008;Wang et al, 2010)? We note that they all utilized fluorescent proteins (GFP and YFP) for cell imaging.…”

“…Because natural selection generally favours early fecundity, the increased death rate evolves as the tradeoff. Recent studies of ageing in Escherichia coli also demonstrate both the acceleration of ageing and the tradeoff (Lindner et al, 2008;Rang et al, 2011;Stewart et al, 2005;Veening et al, 2008). If a mother E. coli cell has non-genetic damage that cannot be repaired, her lineage has a higher evolutionary fitness if she allocates asymmetrically more of the damage to one daughter, rather than symmetrically.…”

“…Recent studies demonstrating ageing or the deterioration of function with time in bacteria recall past debates on immortality, longevity, programmed processes, and the concept of ageing itself (Chao, 2010;Ferber, 2005;Książek, 2010;Lele et al, 2011;Lindner et al, 2008;Nyström, 2002;Rang et al, 2011;Stewart et al, 2005;Turke, 2008;Veening et al, 2008;Wang et al, 2010;Williams, 1957). Discussions of what is biological ageing are often confused because of the existence of several definitions, which we classify as cellular, individual and lineage ageing.…”