Repeated triggering of sporulation in <i>Bacillus subtilis</i> selects against a protein that affects the timing of cell division

Siebring, Jeroen; Elema, Matthijs J. H.; Vega, Fatima Drubi; Kovács, Ákos T.; Haccou, Patsy; Kuipers, Oscar P.

doi:10.1038/ismej.2013.128

Cited by 17 publications

(25 citation statements)

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“…In many regards, capsule switching is reminiscent of both the sporulation process in B . subtilis [ 32 ]—a cell-fate decision that has recently been shown to also be dependent on UDP-glucose levels [ 33 ]—and the phenotypic switch to bacterial persister cells [ 8 , 32 ]. Capsule bistability also shares features with the E .…”

Section: Discussionmentioning

confidence: 99%

Bistability in a Metabolic Network Underpins the De Novo Evolution of Colony Switching in Pseudomonas fluorescens

et al. 2015

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Phenotype switching is commonly observed in nature. This prevalence has allowed the elucidation of a number of underlying molecular mechanisms. However, little is known about how phenotypic switches arise and function in their early evolutionary stages. The first opportunity to provide empirical insight was delivered by an experiment in which populations of the bacterium Pseudomonas fluorescens SBW25 evolved, de novo, the ability to switch between two colony phenotypes. Here we unravel the molecular mechanism behind colony switching, revealing how a single nucleotide change in a gene enmeshed in central metabolism (carB) generates such a striking phenotype. We show that colony switching is underpinned by ON/OFF expression of capsules consisting of a colanic acid-like polymer. We use molecular genetics, biochemical analyses, and experimental evolution to establish that capsule switching results from perturbation of the pyrimidine biosynthetic pathway. Of central importance is a bifurcation point at which uracil triphosphate is partitioned towards either nucleotide metabolism or polymer production. This bifurcation marks a cell-fate decision point whereby cells with relatively high pyrimidine levels favour nucleotide metabolism (capsule OFF), while cells with lower pyrimidine levels divert resources towards polymer biosynthesis (capsule ON). This decision point is present and functional in the wild-type strain. Finally, we present a simple mathematical model demonstrating that the molecular components of the decision point are capable of producing switching. Despite its simple mutational cause, the connection between genotype and phenotype is complex and multidimensional, offering a rare glimpse of how noise in regulatory networks can provide opportunity for evolution.

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Section: Discussionmentioning

confidence: 99%

Bistability in a Metabolic Network Underpins the De Novo Evolution of Colony Switching in Pseudomonas fluorescens

et al. 2015

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“…Formation of an endospore is an expensive dead-end strategy; spore finalization takes approximately 9 hours from initiation [19] and spores do not produce offspring until after germination. Stochastic sporulation initiation without the presence of an environmental cue (starvation) ensures survival in case responsive sporulation lag takes too long and the environmental change is too harmful for sporulation to finalize [20,21].…”

Section: Endospore Formation In B Subtilismentioning

confidence: 99%

Microbial bet-hedging: the power of being different

Grimbergen

Siebring²,

Solopova³

et al. 2015

Current Opinion in Microbiology

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“…Larger chromosomes resulting in decrease in fitness are also observed in endospore-forming Firmicutes: when there is no environmental pressure for sporulation, Firmicutes tend to lose their extra, sporulation-related genes (Callahan et al, 2008; de Hoon et al, 2010). Besides the energetic burden involved in the replication and maintenance of a larger genome, sporulation itself is a costly procedure, chosen only as a last resort adaptation (Ratcliff et al, 2013; Siebring et al, 2014). This would suggest that the biological cost of increased survival might be a better explanation of the distribution patterns of EFF in the environment.…”

Section: Introductionmentioning

confidence: 99%

A Combination of Extreme Environmental Conditions Favor the Prevalence of Endospore-Forming Firmicutes

et al. 2016

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Environmental conditions unsuitable for microbial growth are the rule rather than the exception in most habitats. In response to this, microorganisms have developed various strategies to withstand environmental conditions that limit active growth. Endospore-forming Firmicutes (EFF) deploy a myriad of survival strategies in order to resist adverse conditions. Like many bacterial groups, they can form biofilms and detect nutrient scarcity through chemotaxis. Moreover, within this paraphyletic group of Firmicutes, ecophysiological optima are diverse. Nonetheless, a response to adversity that delimits this group is the formation of wet-heat resistant spores. These strategies are energetically demanding and therefore might affect the biological success of EFF. Therefore, we hypothesize that abundance and diversity of EFF should be maximized in those environments in which the benefits of these survival strategies offsets the energetic cost. In order to address this hypothesis, geothermal and mineral springs and drillings were selected because in these environments of steep physicochemical gradients, diversified survival strategies may become a successful strategy.We collected 71 samples from geothermal and mineral environments characterized by none (null), single or multiple limiting environmental factors (temperature, pH, UV radiation, and specific mineral composition). To measure success, we quantified EFF gene copy numbers (GCN; spo0A gene) in relation to total bacterial GCN (16S rRNA gene), as well as the contribution of EFF to community composition. The quantification showed that relative GCN for EFF reached up to 20% at sites characterized by multiple limiting environmental factors, whereas it corresponded to less than 1% at sites with one or no limiting environmental factor. Pyrosequencing of the 16S rRNA gene supports a higher contribution of EFF at sites with multiple limiting factors. Community composition suggested a combination of phylotypes for which active growth could be expected, and phylotypes that are most likely in the state of endospores, in all the sites. In summary, our results suggest that diversified survival strategies, including sporulation and metabolic adaptations, explain the biological success of EFF in geothermal and natural springs, and that multiple extreme environmental factors favor the prevalence of EFF.

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Repeated triggering of sporulation in Bacillus subtilis selects against a protein that affects the timing of cell division

Cited by 17 publications

References 50 publications

Bistability in a Metabolic Network Underpins the De Novo Evolution of Colony Switching in Pseudomonas fluorescens

Bistability in a Metabolic Network Underpins the De Novo Evolution of Colony Switching in Pseudomonas fluorescens

Microbial bet-hedging: the power of being different

A Combination of Extreme Environmental Conditions Favor the Prevalence of Endospore-Forming Firmicutes

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