Abstract
The discovery of insecticidal activity in root-colonizing pseudomonads, best-known for their plant-beneficial effects, raised fundamental questions about the ecological relevance of insects as alternative hosts for these bacteria. Since soil bacteria are limited in their inherent abilities of dispersal, insects as vectors might be welcome vehicles to overcome large distances. Here, we report on the transmission of the root-colonizing, plant-beneficial and insecticidal bacterium Pseudomonas protegens CHA0 from root to root by the cabbage root fly, Delia radicum. Following ingestion by root-feeding D. radicum larvae, CHA0 persisted inside the insect until the pupal and adult stages. The emerging flies were then able to transmit CHA0 to a new plant host initiating bacterial colonization of the roots. CHA0 did not reduce root damages caused by D. radicum and had only small effects on Delia development suggesting a rather commensal than pathogenic relationship. Interestingly, when the bacterium was fed to two highly susceptible lepidopteran species, most of the insects died, but CHA0 could persist throughout different life stages in surviving individuals. In summary, this study investigated for the first time the interaction of P. protegens CHA0 and related strains with an insect present in their rhizosphere habitat. Our results suggest that plant-colonizing pseudomonads have different strategies for interaction with insects. They either cause lethal infections and use insects as food source or they live inside insect hosts without causing obvious damages and might use insects as vectors for dispersal, which implies a greater ecological versatility of these bacteria than previously thought.
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Acknowledgements
We gratefully acknowledge Matthias Lutz, Jaka Razinger, Anne-Marie Cortesero, Martin Hommes, Syngenta Crop Protection, and the Environmental Systems Sciences group of ETH Zurich for providing insect material. Moreover, we thank Maria Péchy-Tarr and Raphël Groux for the development of the Pieris artificial diet feeding assay. We also thank Ethan Stewart for his help with the measurement of the size of D. radicum pupae by an ImageJ macro. We thank Helga Radke for technical assistance on preparation of insect samples for microscopy and Alexander Rapp from Technical University Darmstadt as well as Astrid Zimmermann for providing anti-GFP antibodies and help on the immunofluorescence microscopy. Furthermore, we acknowledge Johannes Jehle for his support to develop the collaboration between ETH Zurich and JKI Darmstadt. Finally, we thank Dylan Bär, Jana Schneider, Sandra Siegfried, Maria Haller, and Anja Taddei for technical assistance and Tobias Löser and Maria Péchy-Tarr for help with the generation of GFP-tagged strains.
Funding
This study was financed by grants obtained from the Swiss National Foundation for Scientific Research SNSF (Projects 31003A-138248, 31003A-159520, 406840-143141, and 406840-161904). The research stay of PF at JKI Darmstadt and at University of Lausanne were supported by grants obtained from Walter Hochstrasser-Stiftung, Zürich, Switzerland and by the Swiss Plant Science Web, respectively.
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Flury, P., Vesga, P., Dominguez-Ferreras, A. et al. Persistence of root-colonizing Pseudomonas protegens in herbivorous insects throughout different developmental stages and dispersal to new host plants. ISME J 13, 860–872 (2019). https://doi.org/10.1038/s41396-018-0317-4
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DOI: https://doi.org/10.1038/s41396-018-0317-4
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