Control of cell fate by the formation of an architecturally complex bacterial community

Abstract

Bacteria form architecturally complex communities known as biofilms in which cells are held together by an extracellular matrix. Biofilms harbor multiple cell types, and it has been proposed that within biofilms individual cells follow different developmental pathways, resulting in heterogeneous populations. Here we demonstrate cellular differentiation within biofilms of the spore-forming bacterium Bacillus subtilis, and present evidence that formation of the biofilm governs differentiation. We show that motile, matrix-producing, and sporulating cells localize to distinct regions within the biofilm, and that the localization and percentage of each cell type is dynamic throughout development of the community. Importantly, mutants that do not produce extracellular matrix form unstructured biofilms that are deficient in sporulation. We propose that sporulation is a culminating feature of biofilm formation, and that spore formation is coupled to the formation of an architecturally complex community of cells.[Keywords: Bacillus; biofilm; cell fate; development; multicellularity] Supplemental material is available at http://www.genesdev.org.

Single-cell analysis in situ in a Bacillus subtilis swarming community identifies distinct spatially separated subpopulations differentially expressing hag (flagellin), including specialized swarmers

“…The formation of bacterial communities, such as Bacillus subtilis colonies, was shown recently, while this work was in progress, to occur through a developmental-like program, associated with the presence of different cell types (see Vlamakis et al, 2008;Lemon et al, 2008;Ló pez & Kolter, 2010). Another form of community swarming migration over a surface, apparently occurring in thin fluid films, requires flagella, a surfactant and the production of specialized swarmer cells ( , 2008).…”

The predatory life cycle of Myxococcus xanthus

“…xanthus is able to lyse a wide range of Gram-negative and Gram-positive bacteria in a non-species-specific manner (Mendes-Soares & Velicer, 2013). Other soil microbes show cooperative traits, such as Bacillus subtilis, which forms specialized cell types and secretes secondary metabolites that exhibit antibiotic potential at high concentrations (Vlamakis et al, 2008;Liu et al, 2010). However, it is often unclear whether the studied organism actually produces sufficient concentrations of these metabolites for lysis in situ, nor is it obvious whether the organism then derives growth substrates directly from its lysed neighbours.…”

A pivotal role for the response regulator DegU in controlling multicellular behaviour

“…During biofilm formation by B. subtilis, cells differentiate into specific subpopulations that become responsible for matrix production or sporulation (Chai et al, 2008;Vlamakis et al, 2008). This finding suggests that biofilm matrix production altruistically benefits the entire population/community, not just the producer cells.…”

“…Most bacteria exist in their natural habitats as sessile multicellular communities called biofilms in which the bacterial population differentiates as part of the development process (Costerton et al, 1995;Vlamakis et al, 2008). That most bacterial species can live and grow within a shared habitat, and co-ordinate complex group behaviour that benefits the whole community, is still a relatively new concept (Shapiro, 1998).…”

“…Second, developments in the use of fluorescent reporter fusions enable gene expression to be monitored readily within the single cell by flow cytometry. Third, advances in microscopy techniques allow the detection of cell differentiation in an otherwise isogeneic bacterial population (Veening et al, 2004(Veening et al, , 2005Vlamakis et al, 2008).…”