Abstract
Pseudomonas protegens shows a high degree of lifestyle plasticity since it can establish both plant-beneficial and insect-pathogenic interactions. While P. protegens protects plants against soilborne pathogens, it can also invade insects when orally ingested leading to the death of susceptible pest insects. The mechanism whereby pseudomonads effectively switch between lifestyles, plant-beneficial or insecticidal, and the specific factors enabling plant or insect colonization are poorly understood. We generated a large-scale transcriptomics dataset of the model P. protegens strain CHA0 which includes data from the colonization of wheat roots, the gut of Plutella xylostella after oral uptake and the Galleria mellonella hemolymph after injection. We identified extensive plasticity in transcriptomic profiles depending on the environment and specific factors associated to different hosts or different stages of insect infection. Specifically, motor-activity and Reb toxin-related genes were highly expressed on wheat roots but showed low expression within insects, while certain antimicrobial compounds (pyoluteorin), exoenzymes (a chitinase and a polyphosphate kinase), and a transposase exhibited insect-specific expression. We further identified two-partner secretion systems as novel factors contributing to pest insect invasion. Finally, we use genus-wide comparative genomics to retrace the evolutionary origins of cross-kingdom colonization.
Highlights
Pseudomonas is a highly versatile genus that comprises bacteria living in diverse environments and that colonizes
We analyzed the transcriptome of CHA0 after 1 week on wheat roots, when bacteria had established population sizes
P. protegens and P. chlororaphis are bacterial species with multifaceted lifestyles as they can switch between plant and insect hosts
Summary
The ability of P. protegens to colonize cross-kingdom insect and plant hosts is impressively demonstrated by work on the model strain CHA0. It remains largely unknown what specific traits underlie cross-kingdom host colonization and how plastic responses including transcriptional remodeling contribute to switching between hosts. We analyzed the transcriptome of P. protegens CHA0 during the colonization of plant roots, as well as from different compartments of insect hosts, the hemolymph and gut, representing different stages of infection. After 1 week, roots of 99 wheat plants per replicate were harvested, shaken in 0.9% NaCl, the resulting suspensions were centrifuged and pellets containing bacteria were pooled for RNA extraction. The resident cultivable microflora of untreated insects was assessed by growing the extracts on LB media plates at 18, 24, and 37 °C for 1 week
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