Bacterial Discrimination by Dictyostelid Amoebae Reveals the Complexity of Ancient Interspecies Interactions

Amoebae and bacteria interact within predator-prey and host-pathogen relationships, but the general response of amoeba to bacteria is not well understood. The amoeba Dictyostelium discoideum feeds on, and is colonized by, diverse bacterial species, including Gram-positive [Gram(+)] and Gram-negative [Gram(–)] bacteria, two major groups of bacteria that differ in structure and macromolecular composition. Transcriptional profiling of D. discoideum revealed sets of genes whose expression is enriched in amoebae interacting with different species of bacteria, including sets that appear specific to amoebae interacting with Gram(+) or with Gram(–) bacteria. In a genetic screen utilizing the growth of mutant amoebae on a variety of bacteria as a phenotypic readout, we identified amoebal genes that are only required for growth on Gram(+) bacteria, including one that encodes the cell-surface protein gp130, as well as several genes that are only required for growth on Gram(–) bacteria, including one that encodes a putative lysozyme, AlyL. These genes are required for parts of the transcriptional response of wild-type amoebae, and this allowed their classification into potential response pathways. We have defined genes that are critical for amoebal survival during feeding on Gram(+), or Gram(–), bacteria that we propose form part of a regulatory network that allows D. discoideum to elicit specific cellular responses to different species of bacteria in order to optimize survival. •Transcriptional profiling reveals differential responses of amoebae to bacteria•Genetic screens in amoebae reveal potential regulators of bacterial responses•Amoeba appear genetically programmed to respond to Gram(+) or Gram(–) bacteria•A glucose metabolite in amoebae may signal the presence of Gram(+) bacteria