A polarized genome is required for fitness of the obligate intracellular, tick-borne pathogen Rickettsia parkeri

Alphaproteobacteria of the order Rickettsiales include biomedically important, yet understudied arthropod-borne human pathogens. These pathogens lack obvious morphological asymmetry, but encode homologs of key mediators of polar processes in the model Alphaproteobacterium Caulobacter crescentus. These include the polar organizing protein PopZ, the chromosome segregation proteins ParA and ParB, and the spatial regulator of cell division MipZ. Motivated by this observation, we used the tick-borne human pathogen Rickettsia parkeri to ask if the chromosome is polarized and coordinated with cell division in this group. Consistent with that hypothesis, we found that transposon insertion mutants in parA, parB, mipZ, or popZ resulted in cell division defects. Fluorescence imaging revealed cell cycle-dependent unipolar-to-bipolar localization dynamics of ParB and MipZ, and pole-to-midcell dynamics of the division protein ZapA. This patterning parallels the model of chromosome segregation and cell division site selection established in Caulobacter. Unlike its unipolar-to-bipolar dynamics in Caulobacter, however, PopZ remained at a single cell pole throughout the cell cycle in R. parkeri. PopZ maintained its direct interaction with ParA and ParB. Interestingly, disruption of parA or parB, but not popZ or mipZ, caused a small plaque phenotype, suggesting a defect in growth or spread in a monolayer of host cells in the absence of proper chromosome segregation. We propose that genome polarization in R. parkeri and other rickettsiae is critical both for fundamental cellular processes and for interactions with host cells that promote fitness in their infectious niche.