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Evolution of increased virulence is associated with decreased spite in the insect-pathogenic bacterium Xenorhabdus nematophila.

ABSTRACT: Disease virulence may be strongly influenced by social interactions among pathogens, both during the time course of an infection and evolutionarily. Here, we examine how spiteful bacteriocin production in the insect-pathogenic bacterium Xenorhabdus nematophila is evolutionarily linked to its virulence. We expected a negative correlation between virulence and spite owing to their inverse correlations with growth. We examined bacteriocin production and growth across 14 experimentally evolved lineages that show faster host-killing relative to their ancestral population. Consistent with expectations, these more virulent lineages showed reduced bacteriocin production and faster growth relative to the ancestor. Further, bacteriocin production was negatively correlated with growth across the examined lineages. These results strongly support an evolutionary trade-off between virulence and bacteriocin production and lend credence to the view that disease management can be improved by exploiting pathogen social interactions.

SUBMITTER: Bhattacharya A

PROVIDER: S-EPMC6731475 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Evolution of increased virulence is associated with decreased spite in the insect-pathogenic bacterium Xenorhabdus nematophila.

Bhattacharya Amrita A Toro Díaz Valeria C VC Morran Levi T LT Bashey Farrah F

Biology letters 20190828 8

Disease virulence may be strongly influenced by social interactions among pathogens, both during the time course of an infection and evolutionarily. Here, we examine how spiteful bacteriocin production in the insect-pathogenic bacterium Xenorhabdus nematophila is evolutionarily linked to its virulence. We expected a negative correlation between virulence and spite owing to their inverse correlations with growth. We examined bacteriocin production and growth across 14 experimentally evolved linea ...[more]

PMID: 31455168

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Project description:BackgroundXenorhabdus innexi is a bacterial symbiont of Steinernema scapterisci nematodes, which is a cricket-specialist parasite and together the nematode and bacteria infect and kill crickets. Curiously, X. innexi expresses a potent extracellular mosquitocidal toxin activity in culture supernatants. We sequenced a draft genome of X. innexi and compared it to the genomes of related pathogens to elucidate the nature of specialization.ResultsUsing green fluorescent protein-expressing X. innexi we confirm previous reports using culture-dependent techniques that X. innexi colonizes its nematode host at low levels (~3-8 cells per nematode), relative to other Xenorhabdus-Steinernema associations. We found that compared to the well-characterized entomopathogenic nematode symbiont X. nematophila, X. innexi fails to suppress the insect phenoloxidase immune pathway and is attenuated for virulence and reproduction in the Lepidoptera Galleria mellonella and Manduca sexta, as well as the dipteran Drosophila melanogaster. To assess if, compared to other Xenorhabdus spp., X. innexi has a reduced capacity to synthesize virulence determinants, we obtained and analyzed a draft genome sequence. We found no evidence for several hallmarks of Xenorhabdus spp. toxicity, including Tc and Mcf toxins. Similar to other Xenorhabdus genomes, we found numerous loci predicted to encode non-ribosomal peptide/polyketide synthetases. Anti-SMASH predictions of these loci revealed one, related to the fcl locus that encodes fabclavines and zmn locus that encodes zeamines, as a likely candidate to encode the X. innexi mosquitocidal toxin biosynthetic machinery, which we designated Xlt. In support of this hypothesis, two mutants each with an insertion in an Xlt biosynthesis gene cluster lacked the mosquitocidal compound based on HPLC/MS analysis and neither produced toxin to the levels of the wild type parent.ConclusionsThe X. innexi genome will be a valuable resource in identifying loci encoding new metabolites of interest, but also in future comparative studies of nematode-bacterial symbiosis and niche partitioning among bacterial pathogens.

Project description:UnlabelledThe bacterium Xenorhabdus nematophila engages in phenotypic variation with respect to pathogenicity against insect larvae, yielding both virulent and attenuated subpopulations of cells from an isogenic culture. The global regulatory protein Lrp is necessary for X. nematophila virulence and immunosuppression in insects, as well as colonization of the mutualistic host nematode Steinernema carpocapsae, and mediates expression of numerous genes implicated in each of these phenotypes. Given the central role of Lrp in X. nematophila host associations, as well as its involvement in regulating phenotypic variation pathways in other bacteria, we assessed its function in virulence modulation. We discovered that expression of lrp varies within an isogenic population, in a manner that correlates with modulation of virulence. Unexpectedly, although Lrp is necessary for optimal virulence and immunosuppression, cells expressing high levels of lrp were attenuated in these processes relative to those with low to intermediate lrp expression. Furthermore, fixed expression of lrp at high and low levels resulted in attenuated and normal virulence and immunosuppression, respectively, and eliminated population variability of these phenotypes. These data suggest that fluctuating lrp expression levels are sufficient to drive phenotypic variation in X. nematophila.ImportanceMany bacteria use cell-to-cell phenotypic variation, characterized by distinct phenotypic subpopulations within an isogenic population, to cope with environmental change. Pathogenic bacteria utilize this strategy to vary antigen or virulence factor expression. Our work establishes that the global transcription factor Lrp regulates phenotypic variation in the insect pathogen Xenorhabdus nematophila, leading to attenuation of virulence and immunosuppression in insect hosts. Unexpectedly, we found an inverse correlation between Lrp expression levels and virulence: high levels of expression of Lrp-dependent putative virulence genes are detrimental for virulence but may have an adaptive advantage in other aspects of the life cycle. Investigation of X. nematophila phenotypic variation facilitates dissection of this phenomenon in the context of a naturally occurring symbiosis.

Dataset Information

Evolution of increased virulence is associated with decreased spite in the insect-pathogenic bacterium Xenorhabdus nematophila.

Publications

Evolution of increased virulence is associated with decreased spite in the insect-pathogenic bacterium Xenorhabdus nematophila.

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