Hitching a ride in the phyllosphere: Surfactant production of Pseudomonas spp. causes co-swarming of Pantoea eucalypti 299R

Here we demonstrate the beneficial effect of surfactant-producing Pseudomonads on the phyllosphere model strain Pantoea eucalypti 299R. To do so, we conducted a series of experiments in environments of increasing complexity. P. eucalypti 299R and Pseudomonas sp. FF1 (Pff1) or P. eucalypti 299R and the surfactant-deficient mutant P. sp. FF1::{Delta}viscB (Pff1{Delta}viscB) were co-inoculated in broth, on swarming agar plates, and on plants. In broth, there were no differences in the growth dynamics of P. eucalypti 299R when growing in the presence of Pff1 or Pff1{Delta}viscB. By contrast, on swarming agar plates, P. eucalypti was able to co-swarm with Pff1. Co-swarming led to a significant increase in the area colonized and, consequently, a boost in total biomass when compared to P. eucalypti growing with Pff1{Delta}viscB or in monoculture. Finally in planta, there were no significant effects on the population density of P. eucalypti 299R during co-colonization of Arabidopsis thaliana. However, utilizing the single cell bioreporter for reproductive success (CUSPER), we found a temporally distinct beneficial effect of Pff1 on co-inoculated P. eucalypti 299R subpopulations that did not occur in presence of Pff1{Delta}viscB. This led us to formulate a model for the positive effect of surfactant production during leaf colonization. To generalize our results, we tested the effect of three additional surfactant-producing Pseudomonads and their respective surfactant knockout mutants on P. eucalypti 299R on swarming agar. Resulting in similar co-swarming patterns in P. eucalypti 299R and showing that this organism is able to take advantage of competitors during surface colonization. Our results indicate that surfactant-dependent co-motility might be common during leaf colonization and add yet another facet to the already manyfold roles of surfactants.