A localized adaptor protein performs distinct functions at the Caulobacter cell poles

Significance

Asymmetric cell division yields two distinct daughter cells by mechanisms that underlie stem cell behavior and cellular diversity in all organisms. The bacterium Caulobacter crescentus is able to orchestrate this complex process with less than 4,000 genes. This article describes a strategy deployed by Caulobacter where a regulatory protein, PopA, is programed to perform distinct roles based on its subcellular address. We demonstrate that, depending on the availability of a second messenger molecule, PopA adopts either a monomer or dimer form. The two oligomeric forms interact with different partners at the two cell poles, playing a critical role in the degradation of a master transcription factor at one pole and flagellar assembly at the other pole.

Abstract

Asymmetric cell division generates two daughter cells with distinct characteristics and fates. Positioning different regulatory and signaling proteins at the opposing ends of the predivisional cell produces molecularly distinct daughter cells. Here, we report a strategy deployed by the asymmetrically dividing bacterium Caulobacter crescentus where a regulatory protein is programmed to perform distinct functions at the opposing cell poles. We find that the CtrA proteolysis adaptor protein PopA assumes distinct oligomeric states at the two cell poles through asymmetrically distributed c-di-GMP: dimeric at the stalked pole and monomeric at the swarmer pole. Different polar organizing proteins at each cell pole recruit PopA where it interacts with and mediates the function of two molecular machines: the ClpXP degradation machinery at the stalked pole and the flagellar basal body at the swarmer pole. We discovered a binding partner of PopA at the swarmer cell pole that together with PopA regulates the length of the flagella filament. Our work demonstrates how a second messenger provides spatiotemporal cues to change the physical behavior of an effector protein, thereby facilitating asymmetry.