The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in Magnetospirillum gryphiswaldense

Magnetotactic bacteria (MTB) are of special scientific interest due to the formation of magnetosomes, intracellular membrane-enveloped magnetite crystals arranged into a linear chain by a dedicated cytoskeleton. Magnetotaxis relies on the formation and proper inheritance of these unique magnetic organelles, both of which need to be coordinated with the segregation of other cellular content such as chromosomes or motility and chemotaxis related structures. Thus, elaborated mechanisms are required in MTB to coordinate and maintain a high level of spatial and temporal subcellular organization during cytokinesis. However, thus far, underlying mechanisms and polarity determinants such as landmark proteins remained obscure in MTB. Here, we analyzed an ortholog of the polar organizing protein Z in the alphaproteobacterium Magnetospirillum gryphiswaldense termed PopZ(Mgr). We show that deletion of the popZ(Mgr) gene causes abnormal cell elongation, minicell formation, DNA missegregation, and impairs motility. Overproduction of PopZ(Mgr) results in PopZ-rich regions near the poles, which are devoid of larger macromolecules, such as ribosomes, chromosomal DNA, and polyhydroxybutyrate (PHB) granules. Using superresolution microscopy, we show that PopZ(Mgr) exhibits a bipolar localization pattern throughout the cell cycle, indicating that the definition of new poles in M. gryphiswaldense occurs immediately upon completion of cytokinesis. Moreover, substitution of PopZ orthologs between M. gryphiswaldense and the related alphaproteobacterium Caulobacter crescentus indicated that PopZ localization depends on host-specific cues and that both orthologs have diverged to an extent that allows only partial reciprocal functional complementation. Altogether, our results indicate that in M. gryphiswaldense, PopZ plays a critical role during cell division and segregation of cellular content.