Abstract
Cell polarity underlies key processes in all cells, including growth, differentiation and division. In the bacterium Myxococcus xanthus, front-rear polarity is crucial for motility. Notably, this polarity can be inverted, independent of the cell-cycle, by chemotactic signaling. However, a precise understanding of the protein network that establishes polarity and allows for its inversion has remained elusive. Here, we use a combination of quantitative experiments and data-driven theory to unravel the complex interplay between the three key components of the M. xanthus polarity module. By studying each of these components in isolation and their effects as we systematically reconstruct the system, we deduce the network of effective interactions between the polarity proteins. RomR lies at the root of this network, promoting polar localization of the other components, while polarity arises from interconnected negative and positive feedbacks mediated by the small GTPase MglA and its cognate GAP MglB, respectively. We rationalize this network topology as operating as a spatial toggle switch, providing stable polarity for persistent cell movement whilst remaining responsive to chemotactic signaling and thus capable of polarity inversions. Our results have implications not only for the understanding of polarity and motility in M. xanthus but also, more broadly, for dynamic cell polarity.
Highlights
Most cells display an asymmetric distribution of proteins across cellular space that defines a polarity axis [1]
In M. xanthus a well-defined front-rear polarity axis enables efficient translocation. This polarity axis is defined by asymmetric polar localization of a switchlike GTPase and its cognate regulators, and can be reversed in response to signaling cues
Central questions in cell biology are how local molecular interactions result in the polarized distribution of proteins within a cell and how this polarity can be actively changed over time
Summary
Most cells display an asymmetric distribution of proteins across cellular space that defines a polarity axis [1]. Cell polarity is key to processes including growth, division, differentiation and motility [1, 2]. Polarity can be stably maintained over time, as in the apical-basolateral polarity of epithelial cells, and stalked Caulobacter crescentus cells [3, 4]. Polarity can change dynamically in response to external cues, as exemplified by the changing polarity of migrating leukocytes, and front-rear polarity of moving Myxococcus xanthus cells [5, 6]. Central questions in cell biology are how local molecular interactions result in the polarized distribution of proteins within a cell and how this polarity can be actively changed over time. Quantitative data analysis together with data driven modelling have recently been harnessed to uncover the principles that underlie the emergence of polarity [7]
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