Polar accumulation of pyoverdin and exit from stationary phase

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 is induced by arrest of cell division, is achieved by cross-feeding in pyoverdin-nonproducing mutants, is independent of cell shape, and is reversible. Furthermore, it occurs in multi-species communities. Analysis of the performance of pyoverdin-producing and nonproducing cells under conditions promoting polar localization shows an advantage to accumulation on resumption of growth after stress. While the genetic basis of polarization remains unclear, evaluation of deletion mutants of pyoverdin transporters (opmQ, fpvA) establishes non-involvement of these candidate loci. Examination of pyoverdin polar accumulation in a model 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.