Pleiotropic regulation of bacterial toxin production and Allee effect govern microbial predator-prey interactions

Bacteria are social organisms, which are constantly exposed to predation by nematodes or amoebae. To counteract these predation pressures, bacteria have evolved a variety of potent antipredator strategies. Bacteria of the genus Pseudomonas, for instance, evade amoebal predation by the secretion of amoebicidal natural products. The soil bacterium Pseudomonas fluorescens HKI0770 produces pyreudione alkaloids that can kill amoebae. Even though the mode of action of the pyreudiones has been elucidated, the spatiotemporal dynamics underlying this predator-prey interaction remain unknown. Using a combination of microscopy and analytical techniques, we elucidated the intricate relationship of this predator-prey association. We used the chromatic bacteria toolbox for intraspecific differentiation of the amoebicide-producing wildtype and the non-producing mutant within microcosms. These allow for variations in nutrient availability and the emergence of predation-evasion strategies of interacting microorganisms. Imaging of the co-cultures revealed that the amoebae initially ingest both the non-producer as well as the toxin-producer cells. The outcomes of predator-prey interactions are governed by the population size and fitness of the interacting partners. We identified that changes in the cell density coupled with alterations in nutrient availability led to a strong Allee effect resulting in the diminished production of pyreudione A. The loss of defense capabilities renders P. fluorescens HKI0770 palatable to amoebae. Such a multifaceted regulation provides the basis for a model by which predator-prey populations are being regulated in specific niches. Our results demonstrate how the spatiotemporal regulation of bacterial toxin production alters the feeding behavior of amoeba.