Escherichia coli sister cells dynamically organize developmental rosettes

Abstract

Rosettes are self-organizing, circular multicellular communities that initiate the development of organs and embryos in higher organisms. Their formation results from the active repositioning of adhered sister cells and is thought to distinguish multicellular organisms form unicellular ones (1). Though biofilms have been argued to be the result of microbial development (2), bacterial rosettes are uncommon and largely uncharacterized (3-7). Here we report that Escherichia coli rosettes form by a consistent and novel mechanism. After division, sister cells “folded” to reposition themselves in parallel. After the second division, cells folded again to produce clonal 4-cell, quatrefoil rosettes. Analysis of folding revealed that it followed an angular random walk, comprised of ∼1-μm angular strokes and directional randomization. We further showed that this motion was produced by the flagellum, the extracellular tail whose rotation generates swimming motility. Rosette formation was found to require de novo flagella synthesis and the balancing of sister-cell adhesion and propulsion. Moreover, by interrupting sister-cell folding, we demonstrated that rosette formation was required for E. coli’s multicellular-chain life cycle and the resulting clonal-chain biofilms. This study establishes that a unicellular bacterium self-organizes developmental rosettes by active sister-cell repositioning, and has implications for the evolution of multicellularity as well as E. coli’s roles as a commensal and pathogenic organism.