Phenotypic Heterogeneity of the Insect Pathogen Photorhabdus luminescens: Insights into the Fate of Secondary Cells

Photorhabdus luminescens is a Gram-negative bacterium that lives in symbiosis with soil nematodes and is simultaneously highly pathogenic toward insects. The bacteria exist in two phenotypically different forms, designated primary (1 degrees) and secondary (2 degrees) cells. Yet unknown environmental stimuli as well as global stress conditions induce phenotypic switching of up to 50% of 1 degrees cells to 2 degrees cells. An important difference between the two phenotypic forms is that 2 degrees cells are unable to live in symbiosis with nematodes and are therefore believed to remain in the soil after a successful infection cycle. In this work, we performed a transcriptomic analysis to highlight and better understand the role of 2 degrees cells and their putative ability to adapt to living in soil. We could confirm that the major phenotypic differences between the two cell forms are mediated at the transcriptional level as the corresponding genes were downregulated in 2 degrees cells. Furthermore, 2 degrees cells seem to be adapted to another environment as we found several differentially expressed genes involved in the cells' metabolism, motility, and chemotaxis as well as stress resistance, which are either up- or downregulated in 2 degrees cells. As 2 degrees cells, in contrast to 1 degrees cells, chemotactically responded to different attractants, including plant root exudates, there is evidence for the rhizosphere being an alternative environment for the 2 degrees cells. Since P. luminescens is biotechnologically used as a bio-insecticide, investigation of a putative interaction of 2 degrees cells with plants is also of great interest for agriculture. IMPORTANCE The biological function and the fate of P. luminescens 2 degrees cells were unclear. Here, we performed comparative transcriptomics of P. luminescens 1 degrees and 2 degrees cultures and found several genes, not only those coding for known phenotypic differences of the two cell forms, that are up- or downregulated in 2 degrees cells compared to levels in 1 degrees cells. Our results suggest that when 1 degrees cells convert to 2 degrees cells, they drastically change their way of life. Thus, 2 degrees cells could easily adapt to an alternative environment such as the rhizosphere and live freely, independent of a host, putatively utilizing plant-derived compounds as nutrient sources. Since 2 degrees cells are not able to reassociate with the nematodes, an alternative lifestyle in the rhizosphere would be conceivable.