Photorhabdus is a genus of gram-negative Enterobacteriaceae that is pathogenic to insect larvae while also maintaining a mutualistic relationship with nematodes from the family Heterorhabditis, where the bacteria occupy the gut of the infective juvenile (IJ) stage of the nematode. In this study we describe the identification and characterization of a mutation in the pbgE1 gene of Photorhabdus luminescens TT01, predicted to be the fifth gene in the pbgPE operon. We show that this mutant, BMM305, is strongly attenuated in virulence against larvae of the greater wax moth, Galleria mellonella, and we report that BMM305 is more sensitive to the cationic antimicrobial peptide, polymyxin B, and growth in mildly acidic pH than the parental strain of P. luminescens. Moreover, we also show that the lipopolysaccharide (LPS) present on the surface of BMM305 does not appear to contain any O antigen. Complementation studies reveal that the increased sensitivity to polymyxin B and growth in mildly acidic pH can be rescued by the in trans expression of pbgE1, while the defects in O-antigen assembly and pathogenicity require the in trans expression of pbgE1 and the downstream genes pbgE2 and pbgE3. Finally, we show that BMM305 is defective in symbiosis as this mutant is unable to colonize the gut of the IJ stage of the nematode. Therefore, we conclude that the pbgPE operon is required for both pathogenicity and symbiosis in P. luminescens.Photorhabdus is a genus of gram-negative, bioluminescent insect pathogenic bacteria that also has a mutualistic relationship with entomophagous nematodes from the family Heterorhabditis (8). The bacteria colonize the gut of the infective juvenile (IJ) stage of the nematode, a free-living, infectious stage that lives in the soil and actively seeks out insect larvae. The IJ enters the larva and regurgitates the bacteria into the hemolymph, where the bacteria multiply and kill the insect within 24 to 48 h of infection. The bacteria also produce a wide range of extracellular hydrolytic enzymes that function to convert the internal organs and tissues of the insect into a nutrient soup that can support nematode growth and development. After two to three generations within the insect, the nematodes develop into IJs, the bacteria recolonize the intestinal tract, and the IJs emerge from the cadaver in search of a new host (for a recent review, see reference 19).It has been suggested that pathogenicity and symbiosis share common molecular mechanisms and that the outcome of a bacterium-host interaction is the result of a negotiation between the organisms involved in the interaction (28). The Photorhabdus-nematode-insect tripartite system provides a useful model system in which this question can be directly addressed. DNA sequencing has revealed that Photorhabdus contains many genes predicted to encode proteins with homology to virulence factors characterized in other bacterial pathogens (16,20). Recent work has identified the Tc toxin, a large protein complex that is orally active against insect larvae, a...
Pathogenicity and symbiosis are central to bacteria-host interactions. Although several human pathogens have been subjected to functional genomic analysis, we still understand little about bacteria-invertebrate interactions despite their ecological prevalence. Advances in our knowledge of this area are often hindered by the difficulty of isolating and working with invertebrate pathogenic bacteria and their hosts. Here we review studies on pathogenicity and symbiosis in an insect pathogenic bacterium Photorhabdus and its entomopathogenic nematode vector and model insect hosts. Whilst switching between these hosts, Photorhabdus changes from a state of symbiosis with its nematode vector to one of pathogenicity towards its new insect host and both the bacteria and the nematode then cooperatively exploit the dying insect. We examine candidate genes involved in symbiosis and pathogenicity, their secretion and expression patterns in culture and in the host, and begin to dissect the extent of their genetic coregulation. We describe the presence of several large genomic islands, putatively involved in pathogenicity or symbiosis, within the otherwise Yersinia-like backbone of the Photorhabdus genome. Finally, we examine the emerging comparative genomics of the Photorhabdus group and begin to describe the interrelationship between anti-invertebrate virulence factors and those used against vertebrates.
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