Pseudomonas aeruginosa Mobbing-Like Behavior against Acanthamoeba castellanii Bacterivore and Its Rapid Control by Quorum Sensing and Environmental Cues

Abstract

Mobbing, group attack of prey on predator, is a behavior seen in many animal species in which prey animals use numbers and coordination to counter individually superior predators. We studied attack behavior of Pseudomonas aeruginosa toward the bacterivore Acanthamoeba castellanii. This behavior consists of directed motility toward and specific adhesion to the predator cells, enacted in seconds and responding to both prey and predator population densities. Attack coordination relies on remote sensing of the predator and the use of the Pseudomonas quinolone signal (PQS), a P. aeruginosa species-specific quorum sensing molecule. Mutants unable to produce the PQS show unspecific adhesion and reduced survival, and a corresponding increase in predator population occurs as a result of predation. The addition of an external PQS restored some predator-specific adherence within seconds, suggesting a novel response mechanism to this quorum sensing (QS) signal. Fast behavioral response of P. aeruginosa to PQS is also supported by the rate of signal accumulation in the culture, reaching relevant concentrations within minutes, enabling bacteria response to self population density in these short timescales. These results portray a well-regulated group attack of the bacteria against their predator, reacting within seconds to environmental cues and species-specific signaling, which is analogous in many ways to animal mobbing behavior. IMPORTANCE Pseudomonas aeruginosa was shown previously to attack amoebae and other predators by adhering to them and injecting them with virulent substances. In this work, we show that an active, coordinated group behavior is enacted by the bacteria to utilize these molecular components, responding to both predator and bacterial population density. In addition to their ecological significance, immediate behavioral changes observed in response to PQS suggest the existence of a fast QS signal cascade, which is different from canonical QS that relies on slow-to-respond gene regulation. Similar regulatory circuits may drive other bacterial adaptations and pathogenicity mechanisms and may have important clinical implications.