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Abstract

Pyoverdin is a water-soluble metal-chelator synthesized by members of the genus Pseudomonas and used for the acquisition of insoluble ferric iron. Although freely diffusible in aqueous environments, preferential dissemination of pyoverdin among adjacent cells, fine-tuning of intracellular siderophore concentrations, and fitness advantages to pyoverdin-producing versus nonproducing cells, indicate control of location and release. Here, using time-lapse fluorescence microscopy to track single cells in growing microcolonies of Pseudomonas fluorescens SBW25, we show accumulation of pyoverdin at cell poles. Accumulation occurs on cessation of cell growth, is achieved by cross-feeding in pyoverdin-nonproducing mutants and is reversible. Moreover, accumulation coincides with localization of a fluorescent periplasmic reporter, suggesting that pyoverdin accumulation is part of the general cellular response to starvation. Compatible with this conclusion is absence of non-accumulating phenoytpes in a range of pyoverdin mutants. Analysis of the performance of pyoverdin-producing and nonproducing cells under conditions promoting polar accumulation shows an advantage to pyoverdin on resumption of growth after stress. Examination of polar accumulation of pyoverdin in a multispecies community and in a range of laboratory and natural species of Pseudomonas, including P. aeruginosa PAO1 and P. putida KT2440, confirms that the phenotype is characteristic of Pseudomonas.

Significance Statement Bacteria secrete extracellular products that enable nutrients to be obtained from the environment. A secreted product of significance to medicine, agriculture and biotechnology is the iron-chelating siderophore, pyoverdin, produced by members of the genus Pseudomonas. By analyzing the behavior of single cells we show that on cessation of cell division, pyoverdin accumulates at cell poles and does so in periplasmic space created by cytoplasmic shrinkage. The behavior is ecologically relevant: on encountering growth-permissive conditions, cells liberate pyoverdin and exit stationary phase with minimal delay. Our study connects a general biophysical stress response to a molecule of physiological and ecological importance.