SummaryPhotorhabdus and Xenorhabdus bacteria colonize the intestines of the infective soil-dwelling stage of entomophagous nematodes, Heterorhabditis and Steinernema, respectively. These nematodes infect susceptible insect larvae and release the bacteria into the insect blood. The bacteria kill the insect larvae and convert the cadaver into a food source suitable for nematode growth and development. After several rounds of reproduction the nematodes are recolonized by the bacteria before emerging from the insect cadaver into the soil to search for a new host. Photorhabdus and Xenorhabdus bacteria therefore engage in both pathogenic and mutualistic interactions with different invertebrate hosts as obligate components of their life cycle. In this review we aim to describe current knowledge of the molecular mechanisms utilized by Photorhabdus and Xenorhabdus to control their host-dependent interactions. Recent work has established that there is a trade-off between pathogenicity and mutualism in both these species of bacteria suggesting that the transition between these interactions must be under regulatory control. Despite the superficial similarity between the life cycles of these bacteria, it is now apparent that the molecular components of the regulatory networks controlling pathogenicity and mutualism in Photorhabdus and Xenorhabdus are very different.
The bacterium Xenorhabdus nematophila is a mutualist of the entomopathogenic nematode Steinernema carpocapsae. During its life cycle, the bacterium exists both separately from the nematode and as an intestinal resident of a nonfeeding nematode form, the infective juvenile (IJ). The progression of X. nematophila from an ex vivo existence to a specific and persistent colonization of IJs is a model to understand the mechanisms mediating the initiation and maintenance of benign host-microbe interactions. To help characterize this process, we constructed an X. nematophila strain that constitutively expresses green fluorescent protein, which allowed its presence to be monitored within IJs. Using this strain, we showed that few bacterial cells initiate colonization of an individual IJ and that these grow inside the lumen of the IJ intestine in a reproducible polyphasic pattern during colonization. In accordance with these two observations, we demonstrated that the final population of bacteria in a nematode is of predominantly monoclonal origin, suggesting that only one or two bacterial clones initiate or persist during colonization of an individual nematode. These data suggest that X. nematophila initiates IJ colonization by competing for limited colonization sites or resources within the nematode intestine. This report represents the first description of the biological interactions occurring between X. nematophila and S. carpocapsae during the early stages of the colonization process, provides insights into the physiology of X. nematophila in its host niche, and will facilitate interpretation of future data regarding the molecular events mediating this process.The mutualistic, monospecific partnership between the gram-negative enterobacterium Xenorhabdus nematophila and its entomopathogenic nematode host, Steinernema carpocapsae, is one of several emerging models to study benign hostmicrobe interactions (9, 13, 27). The natural life cycle of S. carpocapsae nematodes includes reproductive stages that occur exclusively within larval-stage insects and that are not colonized by X. nematophila and also includes a nonreproductive, nonfeeding, soil-dwelling stage known as the infective juvenile (IJ), which is colonized, at a discrete intestinal location termed the vesicle, by a monoculture of X. nematophila bacteria (9).Colonized IJs exist in the soil until they invade a susceptible insect host, seeking the blood system or hemolymph. Once there, the IJs release their X. nematophila symbionts by defecation (19, 31; E. C. Martens and H. Goodrich-Blair, unpublished data). At this point in their life cycles, bacteria and nematodes exist separately although in close proximity to one another. The released X. nematophila bacteria contribute to the killing of the insect host and grow to high density in the resulting cadaver. These specific bacteria are essential for nematode growth and development presumably both by serving as a direct food source and by supplying nutrients through degradation of the insect carcass (2, 22).When nema...
Comparisons of mutualistic and pathogenic relationships are necessary to decipher the common language of microorganism-host interactions, as well as the subtle differences in dialect that distinguish types of symbiosis. One avenue towards making such comparisons is to study a single organism that speaks both dialects, such as the gamma-proteobacterium Xenorhabdus nematophila. X. nematophila inhabits and influences the lives of two host animals, helping one to reproduce optimally while killing the other.
Members of the genus Xenorhabdus are entomopathogenic bacteria that associate with nematodes. The nematode-bacteria pair infects and kills insects, with both partners contributing to insect pathogenesis and the bacteria providing nutrition to the nematode from available insect-derived nutrients. The nematode provides the bacteria with protection from predators, access to nutrients, and a mechanism of dispersal. Members of the bacterial genus Photorhabdus also associate with nematodes to kill insects, and both genera of bacteria provide similar services to their different nematode hosts through unique physiological and metabolic mechanisms. We posited that these differences would be reflected in their respective genomes. To test this, we sequenced to completion the genomes of Xenorhabdus nematophila ATCC 19061 and Xenorhabdus bovienii SS-2004. As expected, both Xenorhabdus genomes encode many anti-insecticidal compounds, commensurate with their entomopathogenic lifestyle. Despite the similarities in lifestyle between Xenorhabdus and Photorhabdus bacteria, a comparative analysis of the Xenorhabdus, Photorhabdus luminescens, and P. asymbiotica genomes suggests genomic divergence. These findings indicate that evolutionary changes shaped by symbiotic interactions can follow different routes to achieve similar end points.
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