Space and epigenetic inheritance determine inter-individual differences in siderophore gene expression in bacterial colonies

Abstract

AbstractHeterogeneity in gene expression among cells in clonal groups is common in bacteria. Albeit ubiquitous, it often remains unclear what the sources of variation are and whether variation has functional significance. Here, we tracked the expression of genes involved in the synthesis of iron-chelating siderophores (pyoverdine and pyochelin) in individual cells of the bacteriumPseudomonas aeruginosaduring colony growth on surfaces using time-lapse fluorescence microscopy, to explore potential sources and functions of cellular heterogeneity. Regarding sources, we found that the physical position of cells within the colony and epigenetic gene expression inheritance from mother to daughter cells significantly contributed to cellular heterogeneity. In contrast, cell pole age and cellular lifespan had no effect. Regarding functions, our results indicate that cells optimize their siderophore investment strategies (pyoverdine vs. pyochelin) along a gradient from the centre to the edge of the colony. Moreover, we found evidence that cell lineages with above-average siderophore investment increase the fitness of cell lineages with below-average investment through cooperative sharing of secreted siderophores. Altogether, our study highlights that single-cell experiments combined with automated image and cell-tracking analyses can identify sources of heterogeneity and yield adaptive explanations for gene expression variation among clonal bacterial cells.