PATAN‐domain regulators interact with the Type IV pilus motor to control phototactic orientation in the cyanobacterium Synechocystis

Abstract

Many prokaryotes show complex behaviors that require the intricate spatial and temporal organization of cellular protein machineries, leading to asymmetrical protein distribution and cell polarity. One such behavior is cyanobacterial phototaxis which relies on the dynamic localization of the Type IV pilus motor proteins in response to light. In the cyanobacterium Synechocystis, various signaling systems encompassing chemotaxis‐related CheY‐ and PatA‐like response regulators are critical players in switching between positive and negative phototaxis depending on the light intensity and wavelength. In this study, we show that PatA‐type regulators evolved from chemosensory systems. Using fluorescence microscopy and yeast two‐hybrid analysis, we demonstrate that they localize to the inner membrane, where they interact with the N‐terminal cytoplasmic domain of PilC and the pilus assembly ATPase PilB1. By separately expressing the subdomains of the response regulator PixE, we confirm that only the N‐terminal PATAN domain interacts with PilB1, localizes to the membrane, and is sufficient to reverse phototactic orientation. These experiments established that the PATAN domain is the principal output domain of PatA‐type regulators which we presume to modulate pilus extension by binding to the pilus motor components.

Two antagonistic response regulators control Pseudomonas aeruginosa polarization during mechanotaxis

“…The cyanobacterium Synechocystis uses phototaxis to direct T4P‐dependent surface motility. Several chemotaxis‐like systems are involved, three of which encode two response regulators as in Chp (Han et al , 2022 ). The response regulators PixG, PilG, and TaxP2 have an N‐terminal PATAN domain that is missing in PilG of P. aeruginosa and related systems.…”

“…The response regulators PixG, PilG, and TaxP2 have an N‐terminal PATAN domain that is missing in PilG of P. aeruginosa and related systems. The PATAN domain mediates direct interaction with the T4P extension motor PilB, whose localization sets twitching direction in response to light (Schuergers et al , 2015 , 2016 ; Han et al , 2022 ). The output functions of their second response regulators PixH, PilH, and TaxY2 have yet to be resolved, but based on our results in P. aeruginosa , one could anticipate that they counter the function of their cognate first response regulator.…”

Thermosynechococcus switches the direction of phototaxis by a c-di-GMP-dependent process with high spatial resolution

“…In Synechocystis , multiple signalling networks seem to be integrated via PATAN-REC proteins, which interact with PilB1 ( Han et al, 2022 ; Jakob et al, 2020 ). We have not yet assessed the localization of the PilB protein, but we observed that the active pilus filaments face the direction of cell movement ( Figures 7 and 8 ).…”

Pseudomonas aeruginosamechanosensing controls cell polarity during twitching by activating two antagonistic response regulators

“…The cyanobacterium Synechocystis uses phototaxis to direct T4P-dependent surface motility. Several chemotaxis-like systems are involved, three of which comprise two response regulators as in Chp (30). The response regulators PixG, PilG and TaxP2 have an N-terminal PATAN domain that is missing in PilG of P. aeruginosa and related systems.…”

“…The response regulators PixG, PilG and TaxP2 have an N-terminal PATAN domain that is missing in PilG of P. aeruginosa and related systems. The PATAN domain mediates direct interaction with the T4P extension motor PilB whose localization sets twitching direction in response to light (30–32). The output functions of their second response regulators PixH, PilH and TaxY2 have yet to be resolved, but based on our results in P. aeruginosa , one could anticipate that they counter the function of their cognate first response regulator.…”