Paracrine signaling in a bacterium

Abstract

Cellular differentiation is triggered by extracellular signals that cause target cells to adopt a particular fate. Differentiation in bacteria typically involves autocrine signaling in which all cells in the population produce and respond to the same signal. Here we present evidence for paracrine signaling in bacterial populations-some cells produce a signal to which only certain target cells respond. Biofilm formation in Bacillus involves two centrally important signaling molecules, ComX and surfactin. ComX triggers the production of surfactin. In turn, surfactin causes a subpopulation of cells to produce an extracellular matrix. Cells that produced surfactin were themselves unable to respond to it. Likewise, once surfactin-responsive cells commenced matrix production, they no longer responded to ComX and could not become surfactin producers. Insensitivity to ComX was the consequence of the extracellular matrix as mutant cells unable to make matrix responded to both ComX and surfactin. Our results demonstrate that extracellular signaling was unidirectional, with one subpopulation producing a signal and a different subpopulation responding to it. Paracrine signaling in a bacterial population ensures the maintenance, over generations, of particular cell types even in the presence of molecules that would otherwise cause those cells to differentiate into other cell types.

Private link between signal and response in Bacillus subtilis quorum sensing

“…In addition, we observed that a higher fraction of comQ cells activated srfA gene transcription in the presence of ComX than in the undomesticated QS + strains. Bimodal expression of srfA in undomesticated strains was reported previously (19) and was suggested to lead to phenotypic differentiation of the Bacillus population and a division of labor that provide fitness benefits (25). Our results show that the private link between signal production and QS response also has consequences for bimodal expression of srfA in the B. subtilis population.…”

“…3A) was comparable with that of the QS-proficient PS216, which is different from that of domesticated strains. Only PS216 produces surfactin and it was proposed recently that surfactin negatively regulates its own expression (19), which may explain the observed difference in the srfA-expression pattern between domesticated and PS216 derivatives. Interestingly, single-cell microscopy analysis revealed that, despite similar cumulative fluorescence of PS216 and the signal-deficient derivative PS216ΔcomQ in the presence of ComX, the distributions of srfA expression differed between the two strains: in PS216 30 ± 7% of cells did not express srfA-cfp regardless of ComX exposure, but only 14 ± 1% of the mutant population remained uninduced in the presence of ComX (Fig.…”

“…Surfactin is also one of the most effective biosurfactants discovered so far (13)(14)(15); it can penetrate cell membranes of various bacteria (16), inhibit surface adhesion of different pathogens, and act as an antiviral (17,18) or hemolytic agent (18). As surfactin is secreted and affects nonsecretors (19), it can be considered a public good (3,4).…”

Surfactin - Novel Solutions for Global Issues

“…Surfactin production is triggered in a small subset of cells responding to another signalling molecule ComX, which is synthesized by most cells in the population. Surfactin then acts as a paracrine signal that leads to extracellular matrix production in a different subpopulation of cells, which can then no longer respond to ComX and therefore cannot became surfactin producers (Lopez et al, 2009d). The blockage of signalling molecules caused by the extracellular matrix has been reported in eukaryotes to define the distinct cell fates in morphogenesis.…”

A flavin-dependent halogenase catalyzes the chlorination step in the biosynthesis of Dictyostelium differentiation-inducing factor 1

“…For instance, quorum sensing molecules secreted by various bacterial species serve as indicators of local population density and modulate coordinated responses (e.g., luminescence, virulence) in appropriate environmental conditions (4). Bacillus subtilus has also been shown recently to generate a paracrine signal, using the small molecule surfactin to induce differentiation of a subset of cells during biofilm formation (5).…”