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Stochastic pulsing of gene expression enables the generation of spatial patterns in Bacillus subtilis biofilms.

ABSTRACT: Stochastic pulsing of gene expression can generate phenotypic diversity in a genetically identical population of cells, but it is unclear whether it has a role in the development of multicellular systems. Here, we show how stochastic pulsing of gene expression enables spatial patterns to form in a model multicellular system, Bacillus subtilis bacterial biofilms. We use quantitative microscopy and time-lapse imaging to observe pulses in the activity of the general stress response sigma factor σ^B in individual cells during biofilm development. Both σ^B and sporulation activity increase in a gradient, peaking at the top of the biofilm, even though σ^B represses sporulation. As predicted by a simple mathematical model, increasing σ^B expression shifts the peak of sporulation to the middle of the biofilm. Our results demonstrate how stochastic pulsing of gene expression can play a key role in pattern formation during biofilm development.

SUBMITTER: Nadezhdin E

PROVIDER: S-EPMC7031267 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Stochastic pulsing of gene expression enables the generation of spatial patterns in Bacillus subtilis biofilms.

Nadezhdin Eugene E Murphy Niall N Dalchau Neil N Phillips Andrew A Locke James C W JCW

Nature communications 20200219 1

Stochastic pulsing of gene expression can generate phenotypic diversity in a genetically identical population of cells, but it is unclear whether it has a role in the development of multicellular systems. Here, we show how stochastic pulsing of gene expression enables spatial patterns to form in a model multicellular system, Bacillus subtilis bacterial biofilms. We use quantitative microscopy and time-lapse imaging to observe pulses in the activity of the general stress response sigma factor σ<s ...[more]

PMID: 32075967

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Project description:Bacillus subtilis is a soil-dwelling bacterium that can form biofilms, or communities of cells surrounded by a self-produced extracellular matrix. In biofilms, genetically identical cells often exhibit heterogeneous transcriptional phenotypes, so that subpopulations of cells carry out essential yet costly cellular processes that allow the entire population to thrive. Surprisingly, the extent of phenotypic heterogeneity and the relationships between subpopulations of cells within biofilms of even in well-studied bacterial systems like B. subtilis remains largely unknown. To determine relationships between these subpopulations of cells, we created 182 strains containing pairwise combinations of fluorescent transcriptional reporters for the expression state of 14 different genes associated with potential cellular subpopulations. We determined the spatial organization of the expression of these genes within biofilms using confocal microscopy, which revealed that many reporters localized to distinct areas of the biofilm, some of which were co-localized. We used flow cytometry to quantify reporter co-expression, which revealed that many cells "multi-task," simultaneously expressing two reporters. These data indicate that prior models describing B. subtilis cells as differentiating into specific cell types, each with a specific task or function, were oversimplified. Only a few subpopulations of cells, including surfactin and plipastatin producers, as well as sporulating and competent cells, appear to have distinct roles based on the set of genes examined here. These data will provide us with a framework with which to further study and make predictions about the roles of diverse cellular phenotypes in B. subtilis biofilms. IMPORTANCE Many microbes differentiate, expressing diverse phenotypes to ensure their survival in various environments. However, studies on phenotypic differentiation have typically examined only a few phenotypes at one time, thus limiting our knowledge about the extent of differentiation and phenotypic overlap in the population. We investigated the spatial organization and gene expression relationships for genes important in B. subtilis biofilms. In doing so, we mapped spatial gene expression patterns and expanded the number of cell populations described in the B. subtilis literature. It is likely that other bacteria also display complex differentiation patterns within their biofilms. Studying the extent of cellular differentiation in other microbes may be important when designing therapies for disease-causing bacteria, where studying only a single phenotype may be masking underlying phenotypic differentiation relevant to infection outcomes.

Dataset Information

Stochastic pulsing of gene expression enables the generation of spatial patterns in Bacillus subtilis biofilms.

Publications

Stochastic pulsing of gene expression enables the generation of spatial patterns in Bacillus subtilis biofilms.

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