Abstract
Species of Xenorhabdus and Photorhabdus bacteria form mutualistic associations with Steinernema and Heterorhabditis nematodes, respectively and serve as model systems for studying microbe-animal symbioses. Here, we profiled gene expression of Xenorhabdus koppenhoeferi during their symbiotic persistence in the newly formed infective juveniles of the host nematode Steinernema scarabaei through the selective capture of transcribed sequences (SCOTS). The obtained gene expression profile was then compared with other nematode-bacteria partnerships represented by Steinernema carpocapsae—Xenorhabdus nematophila and Heterorhabditis bacteriophora—Photorhabdus temperata. A total of 29 distinct genes were identified to be up-regulated and 53 were down-regulated in X. koppenhoeferi while in S. scarabaei infective juveniles. Of the identified genes, 8 of the up-regulated and 14 of the down-regulated genes were similarly expressed in X. nematophila during persistence in its host nematode S. carpocapsae. However, only one from each of these up- and down-regulated genes was common to the mutualistic partnership between the bacterium P. temperata and the nematode H. bacteriophora. Interactive network analysis of the shared genes between X. koppenhoeferi and X. nematophila demonstrated that the up-regulated genes were mainly involved in bacterial survival and the down-regulated genes were more related to bacterial virulence and active growth. Disruption of two selected genes pta (coding phosphotransacetylase) and acnB (coding aconitate hydratase) in X. nematophila with shared expression signature with X. koppenhoeferi confirmed that these genes are important for bacterial persistence in the nematode host. The results of our comparative analyses show that the two Xenorhabdus species share a little more than a quarter of the transcriptional mechanisms during persistence in their nematode hosts but these features are quite different from those used by P. temperata bacteria in their nematode host H. bacteriophora.
Highlights
Mutualistic associations between entomopathogenic nematodes Steinernema and Heterorhabditis spp. and their symbiotic bacteria Xenorhabdus and Photorhabdus spp. represent one of the best-developed systems for the study of animal-microbe symbiosis [1,2,3]
The patterns of gene expression determined by selective capture of transcribed sequences (SCOTS) were further validated by the Quantitative real-time PCR (qPCR) analysis which showed consistent results on the 14 selected representative genes in X. koppenhoeferi (S2 Fig)
Our in vivo gene expression analysis indicates key molecular features adopted by Xenorhabdus bacteria while in mutualism with their nematode partner
Summary
Mutualistic associations between entomopathogenic nematodes Steinernema and Heterorhabditis spp. and their symbiotic bacteria Xenorhabdus and Photorhabdus spp. represent one of the best-developed systems for the study of animal-microbe symbiosis [1,2,3]. Heterorhabditis and Steinernema belong to phylogenetically distant nematode clades, their symbiotic bacteria Xenorhabdus and Photorhabdus are more closely related to each other [8] and share very similar life histories [9]. The bacteria promote their own transmission among insects by using the nematode infective juvenile as a vector whereas the nematode uses the bacteria as food source [10,11,12]. The bacteria multiply in the hemolymph and produce a plethora of biomolecules [15,16], killing the insect and converting the cadaver into a food source suitable for nematode growth and reproduction. After depleting the insect cadaver the bacteria recolonize the developing infective juveniles that exit the depleted cadaver in search of a new host, ensuring their own transmission to a new insect host using the nematode as a vector [1]
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