Swimming, fast and slow: strategy and survival of bacterial predators in response to chemical cues

Abstract

ABSTRACTBdellovibrio bacteriovorus is a predatory bacterium that preys upon gram-negative bacteria. As such, B. bacteriovorus has the potential to control antibiotic-resistant pathogens and biofilm populations. To survive and reproduce, B. bacteriovorus must locate and infect a host cell. However, in the temporary absence of prey, it is largely unknown how B. bacteriovorus modulate their motility patterns in response to physical or chemical environmental cues to optimize their energy expenditure. To investigate B. bacteriovorus’ predation strategy, we track and quantify their motion by measuring speed distributions and velocity autocorrelations as a function of starvation time. An initial unimodal speed distribution, relaxing to that expected for pure diffusion at long times, may be expected. Instead, we observe a complex, non-Brownian, search strategy as evidenced by distinctly bimodal speed distributions. That is, for an increasing amount of time over which B. bacteriovorus is starved, we observe a progressive re-weighting from a fast mode to a slow mode in the speed distribution obtained over consecutive frames. By contrast to its predator, B. bacteriovorus’ prey, Escherichia coli exhibits almost immediate decrease to a speed expected from passive diffusion following resuspension from rich to poor media. Distributions of trajectory-averaged speeds for B. bacteriovorus are largely unimodal, indicating nontrivial switching between fast and slow swimming modes within individual observed trajectories rather than there being distinct fast and slow populations. We also find that B. bacteriovorus’ slow speed mode is not merely caused by the diffusion of inviable bacteria as subsequent spiking experiments show that bacteria can be resuscitated and bimodality restored. Indeed, starved B. bacteriovorus may modulate the frequency and duration of active swimming as a means of balancing energy consumption and procurement. Our results are evidence of a nontrivial predation strategy, which contrasts with the comparatively simple search pattern of its prey, in response to environmental cues.SIGNIFICANCEBdellovibrio bacteriovorus is a predatory bacterium that is poised to help control gram-negative bacterial populations in environmental and clinical settings. In order to locate its prey in solution, B. bacteriovorus must expend energy in order to fight hydrodynamic drag. This raises the question as to how B. bacteriovorus should expend its energy reserves in the absence of chemical cues from its prey. Here, we show that B. bacteriovorus adapts its motility to minimize energy expenditure (due to fighting drag in swimming) upon prolonged starvation by exploiting two modes of motility. This is in sharp contrast to its prey, E. coli, which shows little active motility under starvation conditions.