Predation Strategies of the Bacterium Bdellovibrio bacteriovorus Result in Overexploitation and Bottlenecks.

With increasing antimicrobial resistance, alternatives for treating infections or removing resistant bacteria are urgently needed, such as the bacterial predator Bdellovibrio bacteriovorus or bacteriophage. Therefore, we need to better understand microbial predator-prey dynamics. We developed mass-action mathematical models of predation for chemostats, which capture the low substrate concentration and slow growth typical for intended application areas of the predators such as wastewater treatment, aquaculture, or the gut. Our model predicted that predator survival required a minimal prey cell size, explaining why Bdellovibrio is much smaller than its prey. A predator considered to be "too good" (attack rate too high, mortality too low) overexploited its prey, leading to extinction (tragedy of the commons). Surprisingly, a predator taking longer to produce more offspring outcompeted a predator producing fewer offspring more rapidly (rate versus yield trade-off). Predation was only efficient in a narrow region around optimal parameters. Moreover, extreme oscillations under a wide range of conditions led to severe bottlenecks. These could be avoided when two prey species became available in alternating seasons. A bacteriophage outcompeted Bdellovibrio due to its higher burst size and faster life cycle. Together, results suggest that Bdellovibrio would struggle to survive on a single prey, explaining why it must be a generalist predator and suggesting it is better suited than phage to environments with multiple prey. IMPORTANCE The discovery of antibiotics led to a dramatic drop in deaths due to infectious disease. Increasing levels of antimicrobial resistance, however, threaten to reverse this progress. There is thus a need for alternatives, such as therapies based on phage and predatory bacteria that kill bacteria regardless of whether they are pathogens or resistant to antibiotics. To best exploit them, we need to better understand what determines their effectiveness. By using a mathematical model to study bacterial predation in realistic slow growth conditions, we found that the generalist predator Bdellovibrio is most effective within a narrow range of conditions for each prey. For example, a minimum prey cell size is required, and the predator should not be "too good," as this would result in overexploitation risking extinction. Together these findings give insights into the ecology of microbial predation and help explain why Bdellovibrio needs to be a generalist predator.