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Aging, immortality and persistence produced by phenotypic heterogeneity in bacterial populations

Abstract

Senescence, the process of age-specific decrease of fitness, has puzzled evolutionary biologists ever since the publication of On the Origin of Species. How ubiquitous among living creatures is this phenotypic decline that arises with age? Up until the last decade aging seemed limited to multicellular organisms with a clear separation between soma and germline, as stated by the Evolutionary Theory of Aging. Bacteria were considered functionally immortal. However, with the improvement of single-cell microscopy techniques, studies revealed that prokaryotes are, indeed, susceptible to aging. Bacteria inheriting a conserved cell pole, harboring larger non-genetic damage loads, display an aging phenotype, while its sibling rejuvenates through the inheritance of a reduced damage load. My research shows that aging and rejuvenation represent deterministic aspects of bacterial physiology, deriving from the stabilization of a population around states of growth equilibrium. The maintenance of this equilibrium allows for proliferative immortality. I demonstrate that equilibrium can be disrupted by extrinsic damage, leading to the mortality of aging lineages while rejuvenating lineages remain immortal. Thus, the phenotypic heterogeneity produced by asymmetric damage partitioning leads to differential mortality in a bacterial population. Finally, I offer evidence for the connection between aging and the phenotype of bacterial persistence, where transiently dormant cells survive antibiotic treatments. This work demonstrates the emergence of deterministic age structures in bacterial populations, its relevance for the maintenance of cellular proliferation, and offers a potential application of this research for a pressing public health concern.

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