Article

Bet-hedging and epigenetic inheritance in bacterial cell development

Molecular Genetics Group, Groningen Biomolecular Sciences and Biotechnology Institute, and Theoretical Biology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, 9751 NN, Haren, The Netherlands.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 04/2008; 105(11):4393-8. DOI: 10.1073/pnas.0700463105
Source: PubMed

ABSTRACT Upon nutritional limitation, the bacterium Bacillus subtilis has the capability to enter the irreversible process of sporulation. This developmental process is bistable, and only a subpopulation of cells actually differentiates into endospores. Why a cell decides to sporulate or not to do so is poorly understood. Here, through the use of time-lapse microscopy, we follow the growth, division, and differentiation of individual cells to identify elements of cell history and ancestry that could affect this decision process. These analyses show that during microcolony development, B. subtilis uses a bet-hedging strategy whereby some cells sporulate while others use alternative metabolites to continue growth, providing the latter subpopulation with a reproductive advantage. We demonstrate that B. subtilis is subject to aging. Nevertheless, the age of the cell plays no role in the decision of its fate. However, the physiological state of the cell's ancestor (more than two generations removed) does affect the outcome of cellular differentiation. We show that this epigenetic inheritance is based on positive feedback within the sporulation phosphorelay. The extended intergenerational "memory" caused by this autostimulatory network may be important for the development of multicellular structures such as fruiting bodies and biofilms.

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    • "In the bacterial population , sporulation does not occur homogenously, but rather occurs in subpopulations. Presumably, this is a bet-hedging strategy that allows the cell to absolutely confirm the need to sporulate prior to engaging in this highly energy-consuming and, once committed, irreversible developmental programme (Veening et al., 2008). The first bet-hedging strategy to delay entry into sporulation is the 'cannibalistic' behaviour displayed by a subpopulation of cells that are the first to detect the onset of starvation conditions. "
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    • "Phenotypic variability, including epigenetic inheritance, also plays an important role in the framework of bet-hedging in which variable populations show increased fitness compared with homogeneous populations in fluctuating environments [39], [40]. However, unlike the concept of bet-hedging, in which population variability maintained in a benign environment serves to rescue the population upon a switch to harsh conditions [36], [41], [42], our phenotypic variations represent exploration toward stabilizing a relaxed, adapted state all within a constant environment. "
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    PLoS ONE 12/2013; 8(12):e81671. DOI:10.1371/journal.pone.0081671 · 3.23 Impact Factor
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    • "Our experimental evolution study aimed to find yet unidentified elements involved in timing and distribution of sporulation initiation in B. subtilis (Maughan and Nicholson, 2004; Veening et al., 2008). "
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    ABSTRACT: Bacillus subtilis sporulation is a last-resort phenotypical adaptation in response to starvation. The regulatory network underlying this developmental pathway has been studied extensively. However, how sporulation initiation is concerted in relation to the environmental nutrient availability is poorly understood. In a fed-batch fermentation set-up, in which sporulation of ultraviolet (UV)-mutagenized B. subtilis is repeatedly triggered by periods of starvation, fitter strains with mutated tagE evolved. These mutants display altered timing of phenotypical differentiation. The substrate for the wall teichoic acid (WTA)-modifying enzyme TagE, UDP-glucose, has recently been shown to be an intracellular proxy for nutrient availability, and influences the timing of cell division. Here we suggest that UDP-glucose also influences timing of cellular differentiation.The ISME Journal advance online publication, 8 August 2013; doi:10.1038/ismej.2013.128.
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