The ComX Quorum Sensing Peptide of Bacillus subtilis Affects Biofilm Formation Negatively and Sporulation Positively

Abstract

Quorum sensing (QS) is often required for the formation of bacterial biofilms and is a popular target of biofilm control strategies. Previous studies implicate the ComQXPA quorum sensing system of Bacillus subtilis as a promoter of biofilm formation. Here, we report that ComX signaling peptide deficient mutants form thicker and more robust pellicle biofilms that contain chains of cells. We confirm that ComX positively affects the transcriptional activity of the PepsA promoter, which controls the synthesis of the major matrix polysaccharide. In contrast, ComX negatively controls the PtapA promoter, which drives the production of TasA, a fibrous matrix protein. Overall, the biomass of the mutant biofilm lacking ComX accumulates more monosaccharide and protein content than the wild type. We conclude that this QS phenotype might be due to extended investment into growth rather than spore development. Consistent with this, the ComX deficient mutant shows a delayed activation of the pre-spore specific promoter, PspoIIQ, and a delayed, more synchronous commitment to sporulation. We conclude that ComX mediated early commitment to sporulation of the wild type slows down biofilm formation and modulates the coexistence of multiple biological states during the early stages of biofilm development.

Fungal–bacterial interaction selects for quorum sensing mutants with increased production of natural antifungal compounds

“…Among many other functions, it has been shown that inactivation of QS can lead to a delay in sporulation entry 36 , which is in accordance with our observation of a reduced sporulation level observed in post-ST variants (Fig.1b). Interestingly, it has been discussed that ComQXPA system may act as a switch that contributes to the stochastic initiation of sporulation which, consequently, is able to achieve a bet-hedging behavior to limit the investment in population growth, and favor commitment to late growth adaptive processes 36 .…”

“…Thus, the enhanced biofilm formation displayed by post-ST variants resulted at first contradictory. However, it has been recently described that B. subtilis strains carrying mutations in genes of the ComQXPA QS system actually form pellicles with more matrix components than the wild-type strain 36 . In fact, ComQXPA mutants are able to develop earlier and thicker biofilms even though with decreased surfactin production.…”

Biofilm Dispersal for Spore Release in Bacillus subtilis

“…Importantly, matrix gene expression in the nascent pellicle is temporally and spatially heterogeneous, after a highly heterogeneous matrix production during initiation of the pellicle, the majority of cells express the genes for matrix production in the middle of biofilm development (around 24 hours) (12). In the later stages, the population becomes heterogeneous again, only a fraction of the cells will produce the matrix (12), while spores also appear (13,14). Such temporal heterogeneity is mirrored by physical heterogeneity; during the initial and later stages of pellicle development, next to a robust, highly matrix-expressing population, a fragile fraction is also present, within which the cell-cell aggregation can be easily disrupted (12).…”

Annulment of antagonism shifts properties that are beneficial to plants in two-member consortia of Bacillus velezensis

“…A loss of antagonisms and the concomitant increase in the production of secondary metabolites that are beneficial to plants (IAA, acetoin, lipopeptides) in coculture (SQR9△spo0A+FZB42) may in part explain the beneficial effect on plants. It has been reported that the amphipathic lipopeptide surfactin acts a 'public good' produced by B. subtilis and that it is necessary for multicellular swarming by reducing the water surface tension (16). In this study, this function may be supplemented by the lipopeptides bacillomycin D and fengycin, which can also act as biosurfactants and could be therefore potential 'public goods' in coculture environments (34).…”

“…The production of public goods by Bacillus, such as extracellular matrix (EPS), siderophores and lipopeptide (e.g. surfactin), are controlled by a quorum sensing system (15,16) and by global transcriptional regulators such as Spo0A and DegU (14,17). Social interactions among Bacillus strains influence the production of public goods at the community level; however, to the best of our knowledge, few studies have focused on how antagonisms or cooperativity affect secretions of lipopeptide antibiotics and plant growth promoting hormones by bacteria in multicellular groups.…”