Analysis of the Inhibition of Sporulation of Bacillus subtilis Caused by Increasing the Number of Copies of the spO0F Gene

Chapman, John W.; Piggot, Patrick J.

doi:10.1099/00221287-133-8-2079

Cited by 7 publications

(7 citation statements)

References 17 publications

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“…However, this result contradicts previous in vivo studies, which indicate that 0F overexpression inhibits sporulation (Chapman and Piggot, 1987; Chastanet et al, 2010; Sen et al, 2011). To resolve this discrepancy, we made a change to the conventionally assumed phosphorelay architecture (Figure 2A without red arrow) and incorporated substrate inhibition of KinA by 0F into the phosphorelay model (red arrow, Figure 2A).…”

Section: Resultscontrasting

confidence: 96%

“…This substrate inhibition effect has been demonstrated previously (Grimshaw et al, 1998), but has received little attention in mathematical modeling studies. This effect is however essential for explaining the inhibitory effect of 0F overexpression on sporulation (Chapman and Piggot, 1987; Chastanet et al, 2010; Sen et al, 2011). Our results demonstrate that this negative feedback based on the substrate inhibition of KinA by 0F plays a critical role in coupling 0A~P pulsing to DNA replication.…”

Section: Discussionmentioning

confidence: 99%

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Chromosomal Arrangement of Phosphorelay Genes Couples Sporulation and DNA Replication

Narula

Kuchina

Lee

et al. 2015

Cell

109

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Summary Genes encoding proteins in a common regulatory network are frequently located close to one another on the chromosome to facilitate co-regulation or couple gene expression to growth rate. Contrasting with these observations, here we demonstrate a functional role for the arrangement of Bacillus subtilis sporulation network genes on opposite sides of the chromosome. We show that the arrangement of two sporulation network genes, one located close to the origin, the other close to the terminus leads to a transient gene dosage imbalance during chromosome replication. This imbalance is detected by the sporulation network to produce cell-cycle coordinated pulses of the sporulation master regulator Spo0A~P. This pulsed response allows cells to decide between sporulation and continued vegetative growth during each cell-cycle spent in starvation. The simplicity of this coordination mechanism suggests that it may be widely applicable in a variety of gene regulatory and stress-response settings.

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Section: Resultscontrasting

confidence: 96%

Section: Discussionmentioning

confidence: 99%

Chromosomal Arrangement of Phosphorelay Genes Couples Sporulation and DNA Replication

Narula

Kuchina

Lee

et al. 2015

Cell

109

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“…Second, as discussed in the model below, there is an additional post-translational “bandpass” regulatory effect due to the dual role of Spo0F, which is required for Spo0A phosphorylation but can also lead to Spo0A dephosphorylation, due to reverse phosphotransfer and the activity of Spo0F phosphatases. These effects can cause net phosphorylation of Spo0A to first increase, and then decrease, as Spo0F levels rise [19]. Third, gene expression during progress to sporulation occurs in a pulse-like fashion every cell cycle [7], [9].…”

Section: Introductionmentioning

confidence: 99%

Dynamical Consequences of Bandpass Feedback Loops in a Bacterial Phosphorelay

2011

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Under conditions of nutrient limitation, Bacillus subtilis cells terminally differentiate into a dormant spore state. Progression to sporulation is controlled by a genetic circuit consisting of a phosphorelay embedded in multiple transcriptional feedback loops, which is used to activate the master regulator Spo0A by phosphorylation. These transcriptional regulatory interactions are “bandpass”-like, in the sense that activation occurs within a limited band of Spo0A∼P concentrations. Additionally, recent results show that the phosphorelay activation occurs in pulses, in a cell-cycle dependent fashion. However, the impact of these pulsed bandpass interactions on the circuit dynamics preceding sporulation remains unclear. In order to address this question, we measured key features of the bandpass interactions at the single-cell level and analyzed them in the context of a simple mathematical model. The model predicted the emergence of a delayed phase shift between the pulsing activity of the different sporulation genes, as well as the existence of a stable state, with elevated Spo0A activity but no sporulation, embedded within the dynamical structure of the system. To test the model, we used time-lapse fluorescence microscopy to measure dynamics of single cells initiating sporulation. We observed the delayed phase shift emerging during the progression to sporulation, while a re-engineering of the sporulation circuit revealed behavior resembling the predicted additional state. These results show that periodically-driven bandpass feedback loops can give rise to complex dynamics in the progression towards sporulation.

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“…Hashiguchi et al (1986) showed that amplification of the tmrA locus resulted in tunicamycin resistance and hyperproduction of a-amylase. Piggot and colleagues also reported the amplification of an integrated plasmid within chromosome (Chapman & Piggot, 1987;Piggot & Curtis, 1987). Wilson & Morgan (1985) demonstrated that gene amplification correlates with the occurrence of tetracycline (Tc) resistance.…”

Section: Introductionmentioning

confidence: 99%

Tetracycline tolerance mediated by gene amplification in Bacillus subtilis

et al. 2014

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Bacillus subtilis can acquire a higher tolerance to tetracycline by increasing the gene dosage of its resistance gene tetB. In this study, we estimated the multiplication effect of tetB on tetracycline tolerance. Cells harbouring multiple copies of tetB were found to comprise approximately 30 % of the total tetracycline-resistant cell population when selected on medium containing 10 mg tetracycline ml "1. Disruption of recA resulted in a significant decrease in the frequency of tetB amplification. Although four direct repeats exist around tetB, the majority of tetB amplicons were found to be flanked by non-homologous sequences, indicating that the initial duplication of tetB can occur largely through RecA-independent recombination. The correlation between the tetB copy number and the MIC values for tetracycline indicated that more than three copies of tetB were required for tolerance to 10 mg tetracycline ml "1 . Thus, the RecA-dependent expansion step appears to be necessary for developing significant tetracycline tolerance mediated by tetB amplification.

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Analysis of the Inhibition of Sporulation of Bacillus subtilis Caused by Increasing the Number of Copies of the spO0F Gene

Cited by 7 publications

References 17 publications

Chromosomal Arrangement of Phosphorelay Genes Couples Sporulation and DNA Replication

Chromosomal Arrangement of Phosphorelay Genes Couples Sporulation and DNA Replication

Dynamical Consequences of Bandpass Feedback Loops in a Bacterial Phosphorelay

Tetracycline tolerance mediated by gene amplification in Bacillus subtilis

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