A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins

Abstract

Stochastic processes are thought to mediate localization of membrane-associated chemotaxis signaling clusters in peritrichous bacteria. Here, we identified a new family of ParA-like ATPases (designated ParC ½for partitioning chemotaxis) encoded within chemotaxis operons of many polar-flagellated g-proteobacteria that actively promote polar localization of chemotaxis proteins. In Vibrio cholerae, a single ParC focus is found at the flagellated old pole in newborn cells, and later bipolar ParC foci develop as the cell matures. The cell cycle-dependent redistribution of ParC occurs by its release from the old pole and subsequent relocalization at the new pole, consistent with a ''diffusion and capture'' model for ParC dynamics. Chemotaxis proteins encoded in the same cluster as ParC have a similar unipolar-to-bipolar transition; however, they reach the new pole after the arrival of ParC. Cells lacking ParC exhibit aberrantly localized foci of chemotaxis proteins, reduced chemotaxis, and altered motility, which likely accounts for their enhanced colonization of the proximal small intestine in an animal model of cholera. Collectively, our findings indicate that ParC promotes the efficiency of chemotactic signaling processes. In particular, ParC-facilitated development of a functional chemotaxis apparatus at the new pole readies this site for its development into a functional old pole after cell division.

ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes

“…S1). A subset of ParA proteins has also been shown to nonspecifically bind DNA as part of their mechanism (3,19). The alignment of PpfA shows suitable residues at the correct positions for predicted DNA binding, and threading PpfA through the Soj structure (6) suggests that these residues would be in the correct orientation to allow for DNA binding.…”

“…The Walker A cytoskeletal P-loop ATPase system is the common mechanism found in plasmid and chromosome segregation, and is typified by the ParA/B system. Genes homologous to parA are also found outside of ParA/B operons, not adjacent to a parB, and are termed orphan ParA systems (2,3). Several of these orphan parA genes are found in the middle of signaling and metabolic operons.…”

“…Several of these orphan parA genes are found in the middle of signaling and metabolic operons. Several of these orphan ParAs have been shown to be involved in the segregation of protein clusters upon division (3)(4)(5); however, their mechanisms of segregation are currently unclear. The proteins displaying ParA-dependent segregation form complexes where precise stoichiometry of the proteins in the complex may be required for accurate function and where each daughter cell needs to contain that protein complex immediately upon cell division.…”

“…Homologous orphan parA genes have been identified in over 53% of chemotaxis operons. Orphan parA genes have also been shown to control the localization of polar chemotaxis proteins in Vibrio cholera, in this case probably using a system related to the PopZ system of chromosome segregation (3). Bioinformatic analysis has suggested that there may be a number of distinct clades of Par-like orphan systems (3), probably using different mechanisms to segregate membrane and cytoplasmic complexes.…”

“…From our analysis of published genomes, most bacterial genomes encode an orphan parA, and species can contain between 1 and 10 orphan parA genes. Bioinformatic analysis suggests that some orphan Par systems are likely to work like plasmid partition systems (3).…”