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Analyses of competent and non-competent subpopulations of Bacillus subtilis reveal yhfW, yhxC and ncRNAs as novel players in competence.

ABSTRACT: Upon competence-inducing nutrient-limited conditions, only part of the Bacillus subtilis population becomes competent. Here, we separated the two subpopulations by fluorescence-assisted cell sorting (FACS). Using RNA-seq, we confirmed the previously described ComK regulon. We also found for the first time significantly downregulated genes in the competent subpopulation. The downregulated genes are not under direct control by ComK but have higher levels of corresponding antisense RNAs in the competent subpopulation. During competence, cell division and replication are halted. By investigating the proteome during competence, we found higher levels of the regulators of cell division, MinD and Noc. The exonucleases SbcC and SbcD were also primarily regulated at the post-transcriptional level. In the competent subpopulation, yhfW was newly identified as being highly upregulated. Its absence reduces the expression of comG, and has a modest, but statistically significant effect on the expression of comK. Although expression of yhfW is higher in the competent subpopulation, no ComK-binding site is present in its promoter region. Mutants of yhfW have a small but significant defect in transformation. Metabolomic analyses revealed significant reductions in tricarboxylic acid (TCA) cycle metabolites and several amino acids in a ΔyhfW mutant. RNA-seq analysis of ΔyhfW revealed higher expression of the NAD synthesis genes nadA, nadB and nadC.

SUBMITTER: Boonstra M

PROVIDER: S-EPMC7317962 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Analyses of competent and non‐competent subpopulations of Bacillus subtilis reveal yhfW, yhxC and ncRNAs as novel players in competence

Project description:Upon competence‐inducing nutrient‐limited conditions, only part of the Bacillus subtilis population becomes competent. Here, we separated the two subpopulations by fluorescence‐assisted cell sorting (FACS). Using RNA‐seq, we confirmed the previously described ComK regulon. We also found for the first time significantly downregulated genes in the competent subpopulation. The downregulated genes are not under direct control by ComK but have higher levels of corresponding antisense RNAs in the competent subpopulation. During competence, cell division and replication are halted. By investigating the proteome during competence, we found higher levels of the regulators of cell division, MinD and Noc. The exonucleases SbcC and SbcD were also primarily regulated at the post‐transcriptional level. In the competent subpopulation, yhfW was newly identified as being highly upregulated. Its absence reduces the expression of comG, and has a modest, but statistically significant effect on the expression of comK. Although expression of yhfW is higher in the competent subpopulation, no ComK‐binding site is present in its promoter region. Mutants of yhfW have a small but significant defect in transformation. Metabolomic analyses revealed significant reductions in tricarboxylic acid (TCA) cycle metabolites and several amino acids in a ΔyhfW mutant. RNA‐seq analysis of ΔyhfW revealed higher expression of the NAD synthesis genes nadA, nadB and nadC.

2021-04-30 | GSE173540 | GEO

Analyses of competent and non‐competent subpopulations of Bacillus subtilis reveal yhfW, yhxC and ncRNAs as novel players in competence

Project description:Analyses of competent and non‐competent subpopulations of Bacillus subtilis reveal yhfW, yhxC and ncRNAs as novel players in competence

| PRJNA726040 | ENA

Genetic Competence Drives Genome Diversity in Bacillus subtilis.

Project description:Prokaryote genomes are the result of a dynamic flux of genes, with increases achieved via horizontal gene transfer and reductions occurring through gene loss. The ecological and selective forces that drive this genomic flexibility vary across species. Bacillus subtilis is a naturally competent bacterium that occupies various environments, including plant-associated, soil, and marine niches, and the gut of both invertebrates and vertebrates. Here, we quantify the genomic diversity of B. subtilis and infer the genome dynamics that explain the high genetic and phenotypic diversity observed. Phylogenomic and comparative genomic analyses of 42 B. subtilis genomes uncover a remarkable genome diversity that translates into a core genome of 1,659 genes and an asymptotic pangenome growth rate of 57 new genes per new genome added. This diversity is due to a large proportion of low-frequency genes that are acquired from closely related species. We find no gene-loss bias among wild isolates, which explains why the cloud genome, 43% of the species pangenome, represents only a small proportion of each genome. We show that B. subtilis can acquire xenologous copies of core genes that propagate laterally among strains within a niche. While not excluding the contributions of other mechanisms, our results strongly suggest a process of gene acquisition that is largely driven by competence, where the long-term maintenance of acquired genes depends on local and global fitness effects. This competence-driven genomic diversity provides B. subtilis with its generalist character, enabling it to occupy a wide range of ecological niches and cycle through them.

| S-EPMC5765554 | biostudies-literature

Impact of nanoparticles on the Bacillus subtilis (3610) competence.

Project description:Due to the physicochemical properties of nanoparticles, the use of nanomaterials increases every year in industrial and medical processes. At the same time, the increasing number of bacteria becoming resistant to many antibiotics, mostly by a horizontal gene transfer process, is a major public health concern. We herein report, for the first time, the role of nanoparticles in the physiological induction of horizontal gene transfer in bacteria. Besides the most well-known impacts of nanoparticles on bacteria, i.e. death or oxidative stress, two nanoparticles, n-ZnO and n-TiO2, significantly and oppositely impact the transformation efficiency of Bacillus subtilis in biofilm growth conditions, by modification of the physiological processes involved in the induction of competence, the first step of transformation. This effect is the consequence of a physiological adaptation rather than a physical cell injury: two oligopeptide ABC transporters, OppABCDF and AppDFABC, are differentially expressed in response to nanoparticles. Interestingly, a third tested nanoparticle, n-Ag, has no significant effect on competence in our experimental conditions. Overall, these results show that nanoparticles, by altering bacterial physiology and especially competence, may have profound influences in unsuspected areas, such as the dissemination of antibiotic resistance in bacteria.

| S-EPMC5813000 | biostudies-literature

Fitness Trade-Offs in Competence Differentiation of Bacillus subtilis.

Project description:In the stationary phase, Bacillus subtilis differentiates stochastically and transiently into the state of competence for transformation (K-state). The latter is associated with growth arrest, and it is unclear how the ability to develop competence is stably maintained, despite its cost. To quantify the effect differentiation has on the competitive fitness of B. subtilis, we characterized the competition dynamics between strains with different probabilities of entering the K-state. The relative fitness decreased with increasing differentiation probability both during the stationary phase and during outgrowth. When exposed to antibiotics inhibiting cell wall synthesis, transcription, and translation, cells that differentiated into the K-state showed a selective advantage compared to differentiation-deficient bacteria; this benefit did not require transformation. Although beneficial, the K-state was not induced by sub-MIC concentrations of antibiotics. Increasing the differentiation probability beyond the wt level did not significantly affect the competition dynamics with transient antibiotic exposure. We conclude that the competition dynamics are very sensitive to the fraction of competent cells under benign conditions but less sensitive during antibiotic exposure, supporting the picture of stochastic differentiation as a fitness trade-off.

| S-EPMC4896167 | biostudies-literature

Agent-based modeling of competence phenotype switching in Bacillus subtilis.

Project description:BackgroundIt is a fascinating phenomenon that in genetically identical bacteria populations of Bacillus subtilis, a distinct DNA uptake phenotype called the competence phenotype may emerge in 10-20% of the population. Many aspects of the phenomenon are believed to be due to the variable expression of critical genes: a stochastic occurrence termed "noise" which has made the phenomenon difficult to examine directly by lab experimentation.MethodsTo capture and model noise in this system and further understand the emergence of competence both at the intracellular and culture levels in B. subtilis, we developed a novel multi-scale, agent-based model. At the intracellular level, our model recreates the regulatory network involved in the competence phenotype. At the culture level, we simulated growth conditions, with our multi-scale model providing feedback between the two levels.ResultsOur model predicted three potential sources of genetic "noise". First, the random spatial arrangement of molecules may influence the manifestation of the competence phenotype. In addition, the evidence suggests that there may be a type of epigenetic heritability to the emergence of competence, influenced by the molecular concentrations of key competence molecules inherited through cell division. Finally, the emergence of competence during the stationary phase may in part be due to the dilution effect of cell division upon protein concentrations.ConclusionsThe competence phenotype was easily translated into an agent-based model - one with the ability to illuminate complex cell behavior. Models such as the one described in this paper can simulate cell behavior that is otherwise unobservable in vivo, highlighting their potential usefulness as research tools.

| S-EPMC3648451 | biostudies-literature

Molecular level stochastic model for competence cycles in Bacillus subtilis.

Project description:The role of stochasticity and noise in controlling genetic circuits is investigated in the context of transitions into and from competence in Bacillus subtilis. Recent experiments have demonstrated that bistability is not necessary for this function, but that the existence of one stable fixed point (vegetation) and an excitable unstable one (competence) is sufficient. Stochasticity therefore plays a crucial role in this excitation. Noise can be generated by discrete events such as RNA and protein synthesis and their degradation. We consider an alternative noise source connected with the protein binding/unbinding to the DNA. A theoretical model that includes this "nonadiabatic" mechanism appears to produce a better agreement with experiments than models where only the adiabatic limit is considered, suggesting that this nonconventional stochasticity source may be important for biological functions.

| S-EPMC2077070 | biostudies-literature

Time-resolved transcriptomics and bioinformatic analyses reveal intrinsic stress responses during batch culture of Bacillus subtilis.

Project description:We have determined the time-resolved transcriptome of the model gram-positive organism B. subtilis during growth in a batch fermentor on rich medium. DNA microarrays were used to monitor gene transcription using 10-minute intervals at 40 consecutive time points. From the growth curve and analysis of all gene expression levels, we identified 4 distinct growth phases and one clear transition point: a lag phase, an exponential growth phase, the transition point and the very clearly separated early and late stationary growth phases. The gene expression profiles suggest the occurrence of stress responses at specific times although no external stresses were applied. The first one is a small induction of the SigB regulon that occurs at the transition point. Remarkably, a very strong response is observed for the SigW regulon, which is highly upregulated at the onset of the late stationary phase. Bioinformatic analyses that were performed on our data set suggest several novel putative motifs for regulator binding. In addition, the expression profiles of several genes appeared to correlate with the oxygen concentration. This data set of the expression profiles of all B. subtilis genes during the entire growth curve on rich medium constitutes a rich repository that can be further mined by the scientific community.

| S-EPMC3210768 | biostudies-literature

Noise Expands the Response Range of the Bacillus subtilis Competence Circuit.

Project description:Gene regulatory circuits must contend with intrinsic noise that arises due to finite numbers of proteins. While some circuits act to reduce this noise, others appear to exploit it. A striking example is the competence circuit in Bacillus subtilis, which exhibits much larger noise in the duration of its competence events than a synthetically constructed analog that performs the same function. Here, using stochastic modeling and fluorescence microscopy, we show that this larger noise allows cells to exit terminal phenotypic states, which expands the range of stress levels to which cells are responsive and leads to phenotypic heterogeneity at the population level. This is an important example of how noise confers a functional benefit in a genetic decision-making circuit.

| S-EPMC4803322 | biostudies-literature

Deciding fate in adverse times: sporulation and competence in Bacillus subtilis.

Project description:Bacteria serve as the central arena for understanding how gene networks and proteins process information and control cellular behaviors. Recently, much effort has been devoted to the investigation of specific bacteria gene circuits as functioning modules. The next challenge is the integrative modeling of complex cellular networks composed of many such modules. A tractable integrative model of the sophisticated decision-making signal transduction system that determines the fate between sporulation and competence is presented. This model provides an understanding of how information is sensed and processed to reach an "informative" decision in the context of cell state and signals from other cells. The competence module (ComK dynamics) is modeled as a stochastic switch whose transition rate is controlled by a quorum-sensing unit. The sporulation module (Spo0A dynamics) is modeled as a timer whose clock rate is adjusted by a stress-sensing unit. The interplay between these modules is mediated via the Rap assessment system, which gates the sensing units, and the AbrB-Rok decision module, which creates an opportunity for competence within a specific window of the sporulation timer. The timer is regulated via a special repressilator-like inhibition of Spo0A* by Spo0E, which is itself inhibited by AbrB. For some stress and input signals, this repressilator can generate a frustration state with large variations (fluctuations or oscillations) in Spo0A* and AbrB concentrations, which might serve an important role in generating cell variability. This integrative framework is a starting point that can be extended to include transition into cannibalism and the role of colony organization.

| S-EPMC2795487 | biostudies-literature

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