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    Pulcherrimin formation controls growth arrest of the Bacillus subtilis biofilm

    Year: 2019

    Journal: Proc. Natl. Acad. Sci. U. S. A., Volume 116, JUL 2, page 13553–13562

    Authors: Arnaouteli, Sofia; Matoz-Fernandez, D. A.; Porter, Michael; Kalamara, Margarita; Abbott, James; MacPhee, Cait E.; Davidson, Fordyce A.; Stanley-Wall, Nicola R.

    Organizations: Biotechnology and Biological Sciences Research CouncilUK Research & Innovation (UKRI)Biotechnology and Biological Sciences Research Council (BBSRC) [BB/P001335/1, BB/R012415/1, BB/M010996/1]; Wellcome Trust Technology Platform AwardWellcome Trust [097945/B/11/Z]; MRC Next Generation Optical Microscopy AwardUK Research & Innovation (UKRI)Medical Research Council UK (MRC) [MR/K015869/1]

    Keywords: Bacillus subtilis; growth arrest; biofilm; pulcherrimin

    Biofilm formation by Bacillus subtilis is a communal process that culminates in the formation of architecturally complex multicellular communities. Here we reveal that the transition of the biofilm into a nonexpanding phase constitutes a distinct step in the process of biofilmdevelopment. Using genetic analysis we show that B. subtilis strains lacking the ability to synthesize pulcherriminic acid form biofilms that sustain the expansion phase, thereby linking pulcherriminic acid to growth arrest. However, production of pulcherriminic acid is not sufficient to block expansion of the biofilm. It needs to be secreted into the extracellular environment where it chelates Fe3+ from the growth medium in a nonenzymatic reaction. Utilizing mathematical modeling and a series of experimental methodologies we show that when the level of freely available iron in the environment drops below a critical threshold, expansion of the biofilm stops. Bioinformatics analysis allows us to identify the genes required for pulcherriminic acid synthesis in other Firmicutes but the patchwork presence both within and across closely related species suggests loss of these genes through multiple independent recombination events. The seemingly counterintuitive self-restriction of growth led us to explore if there were any benefits associated with pulcherriminic acid production. We identified that pulcherriminic acid producers can prevent invasion by neighboring communities through the generation of an "iron-free" zone, thereby addressing the paradox of pulcherriminic acid production by B. subtilis.
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