Evolutionary repurposing of a DNA segregation machinery into a cytoskeletal system controlling cyanobacterial cell shape
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Bacteria, despite their diversity, use conserved cytoskeletal systems for their intracellular organization. In unicellular bacteria, the ParMRC DNA partitioning apparatus is well known for forming actin-like filaments that push low copy number plasmids to opposite cell poles. In multicellular cyanobacteria such as Anabaena sp. PCC 7120, the presence of a chromosomally encoded ParMR system suggests it may play an analogous role in chromosome segregation. However, we show here that it instead constitutes a novel cytoskeletal system – termed CorMR – whose loss does not impair DNA segregation but leads to severe morphological defects, revealing a role in maintaining cell shape. Using live-cell imaging and in vitro reconstitution experiments, we demonstrate that CorM forms dynamically instable filaments. These filaments are recruited to the membrane by CorR, which has acquired a conserved N-terminal amphipathic helix specific to multicellular cyanobacteria. Cryo-EM analysis reveals that CorM forms antiparallel double-stranded filaments, in contrast to the polar, parallel filament pair seen in ParM. Furthermore, CorMR filaments are excluded from the cell poles and division plane by MinC, via a long N-terminal extension also specific to multicellular cyanobacteria. Comparative genomics suggests that cyanobacterial multicellularity co-evolved with the chromosomal relocation of ParMR genes, acquisition of the amphipathic helix in CorR, and functional extension of MinC, supporting an evolutionary link among these features. Our findings uncover a striking repurposing of ancestral biochemical systems, expanding the known roles of ParMR and Min systems beyond plasmid segregation and division site selection to include regulation of cell shape.
Importance
The ParMRC system is a well-characterized machinery for the segregation of low-copy-number plasmids to the cell poles and, until now, was primarily described to be encoded on plasmids. We found that during the emergence of multicellularity in cyanobacteria, a chromosome-encoded ParMR system has undergone extensive evolutionary and functional repurposing, resulting in a previously undescribed bacterial cytoskeletal system that controls cell shape. We also found that this new cytoskeleton, called CorMR, is under the control of the MinCDE system, which has evolved to not only antagonize Z-ring formation, but also to regulate CorM polymerization. Such interplay between different cytoskeletal systems highlights an intricate regulatory mechanism linking cell division and morphology. As this repurposing of existing cytoskeletal system coincided with the emergence of multicellularity in cyanobacteria, it may have played a key role for the evolution of cyanobacteria with distinct cell shapes. Overall, our discovery highlights the plasticity of bacterial polymeric systems and gives insight into the evolution of cellular and multicellular complexity.
