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.
Significance Bacteria secrete extracellular products that enable nutrients to be obtained from the environment. A secreted product of relevance for medicine, agriculture and biotechnology is the iron-chelating siderophore, pyoverdin, which is produced by members of the genus Pseudomonas. By analyzing the behavior of single cells we show that on cessation of cell division, pyoverdin localizes to cell poles, but is then released to the environment prior to resumption of cell growth. Of particular significance is the ecological relevance of this behavior: cells that accumulate the siderophore resume growth with minimal delay. Our study reveals a hitherto unrecognized dimension to the biology of Pseudomonas that may prove central to understanding the broader ecological and physiological relevance of pyoverdin.
Competing Interest Statement
The authors have declared no competing interest.