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Genes & Dev. 25 (14): 1544-1555

Copyright © 2011 by Cold Spring Harbor Laboratory Press.

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

Simon Ringgaard1,2,3, Kathrin Schirner2, Brigid M. Davis1,2,3,, and Matthew K. Waldor1,2,3,4

1 Channing Laboratory, Brigham and Women's Hospital, Boston, Massachusetts 02115, USA;
2 Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA;
3 Howard Hughes Medical Institute, Boston, Massachusetts 02115, USA

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 [for partitioning chemotaxis]) encoded within chemotaxis operons of many polar-flagellated {gamma}-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.

Key Words: chemotaxis • cell pole maturation • protein localization • bacterial development • ParA • ATPase

Received for publication April 21, 2011. Accepted for publication June 3, 2011.

4 Corresponding author.

E-mail mwaldor{at}rics.bwh.harvard.edu.

Supplemental material is available for this article.

Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.2061811.

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
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A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole.
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ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes.
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