Photosensing and quorum sensing are integrated to control Pseudomonas aeruginosa collective behaviors

Abstract

Bacteria convert changes in sensory inputs into alterations in gene expression, behavior, and lifestyles. A common lifestyle choice that bacteria make is whether to exhibit individual behavior and exist in the free-living planktonic state or to engage in collective behavior and form sessile communities called biofilms. Transitions between individual and collective behaviors are controlled by the chemical cell-to-cell communication process called quorum sensing. Here, we show that quorum sensing represses Pseudomonas aeruginosa biofilm formation and virulence by activating expression of genes encoding the KinB–AlgB two-component system (TCS). Phospho-AlgB represses biofilm and virulence genes, while KinB dephosphorylates and thereby inactivates AlgB. We discover that the photoreceptor BphP is the kinase that, in response to light, phosphorylates and activates AlgB. Indeed, exposing P. aeruginosa to light represses biofilm formation and virulence gene expression. To our knowledge, P. aeruginosa was not previously known to detect and respond to light. The KinB–AlgB–BphP module is present in all pseudomonads, and we demonstrate that AlgB is the partner response regulator for BphP in diverse bacterial phyla. We propose that in the KinB–AlgB–BphP system, AlgB functions as the node at which varied sensory information is integrated. This network architecture provides a mechanism enabling bacteria to integrate at least two different sensory inputs, quorum sensing (via RhlR-driven activation of algB) and light (via BphP–AlgB), into the control of collective behaviors. This study sets the stage for light-mediated control of P. aeruginosa infectivity.

Collective Dynamics of Model Pili-Based Twitcher-Mode Bacilliforms

“…While our model is simplified compared to the biological complexity of P. aeruginosa and other bacteria that employ twitching as a motility strategy, microscopic details of swimming motility have previously been shown to result in qualitative changes to collective dynamics 26,[91][92][93] and swarming-mode motility of P. aeruginosa 94 . Our well defined microscopic model of the twitching mode motility cycle captures the essential microscopic details that differentiate biologically relevant twitching motility from a purely idealized toy model of self-propelled rods and demonstrates that twitching motility is sufficient to exhibit physically mediated collectivity, without requiring additional long-range complications, such as photosensing and quorum sensing 95 or secretions 56 or other forms of bacterial stigmergy 96 . Although lacking a clear signal in the first order statistics of mean squared displacement, the collectivity of twitchers above a critical coverage fraction can be directly quantified by higher order statistics, including the non-Gaussian parameter, decorrelation lengths and the scaling of the fluctuations with local coverage.…”

Pseudomonas aeruginosa biofilm formation on endotracheal tubes requires multiple two-component systems

“…3, Table S1). Recent reports suggest that KinB regulates pelA transcription and is necessary for colony biofilm on congo red agar medium [74]. These five TCSs (FleR, FleS, PhoQ, AlgR and KinB) may be the core requirement of biofilm formation on solid surfaces.…”

A High-Throughput Method for Identifying Novel Genes That Influence Metabolic Pathways Reveals New Iron and Heme Regulation in Pseudomonas aeruginosa

“…HemO cleaves heme to yield biliverdin (BV) IXδ, enabling iron extraction ( 10 ). P. aeruginosa also possesses another heme oxygenase, BphO, that serves to convert heme to BV IXα, which is then attached to the phytochrome light receptor to enable far-red-light detection, and the subsequent modulation of biofilm formation and possibly virulence ( 11 ).…”