Lifecycle of a predatory bacterium vampirizing its prey through the cell envelope and S-layer

Abstract

Predatory bacteria feed upon and kill other bacteria in various natural environments. Obligate epibiotic predators like Bdellovibrio exovorus consume their prey whilst remaining attached to the outside of the prey. How these predators achieve epibiotic feeding through the prey cell envelope has not been explored previously. Whereas the S-layer is the only proposed defensive structure against predatory bacteria, it remains unclear how this thin outer layer of the envelope might prevent epibiotic attacks. Similarly, the lifecycle of B. exovorus during the predator-prey interaction is poorly understood, with current models suggesting a binary division. Here we imaged the entire predatory lifecycle of B. exovorus and the fate of its Caulobacter crescentus prey by time-lapse microscopy and cryo-electron microscopy to monitor predator attack, growth and division and assess the impact of the S-layer on epibiotic predation. Our data reveal that B. exovorus uses non-binary division in a novel proliferation pattern that mainly generates three progenies. Moreover, we found that B. exovorus predates regardless of the presence of an S-layer, calling for revisiting its protective role against predators. Finally, our results indicate that epibiotic predation relies on the establishment of a secured junction between the prey and predator outer membranes, which must be resolved unilaterally to maintain cellular integrity of the predator departing from the prey surface.