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CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila.

ABSTRACT: The CpxRA signal transduction system, which in Escherichia coli regulates surface structure assembly and envelope maintenance, is involved in the pathogenic and mutualistic interactions of the entomopathogenic bacterium Xenorhabdus nematophila. When DeltacpxR1 cells were injected into Manduca sexta insects, the time required to kill 50% of the insects was twofold longer than the time observed for wild-type cells and the DeltacpxR1 cells ultimately killed 16% fewer insects than wild-type cells killed. During mutualistic colonization of Steinernema carpocapsae nematodes, the DeltacpxR1 mutant achieved colonization levels that were only 38% of the wild-type levels. DeltacpxR1 cells exhibited an extended lag phase when they were grown in liquid LB or hemolymph, formed irregular colonies on solid medium, and had a filamentous cell morphology. A mutant with a cpxRp-lacZ fusion had peaks of expression in the log and stationary phases that were conversely influenced by CpxR; the DeltacpxR1 mutant produced 130 and 17% of the wild-type beta-galactosidase activity in the log and stationary phases, respectively. CpxR positively influences motility and secreted lipase activity, as well as transcription of genes necessary for mutualistic colonization of nematodes. CpxR negatively influences the production of secreted hemolysin, protease, and antibiotic activities, as well as the expression of mrxA, encoding the pilin subunit. Thus, X. nematophila CpxRA controls expression of envelope-localized and secreted products, and its activity is necessary for both mutualistic and pathogenic functions.

SUBMITTER: Herbert EE

PROVIDER: S-EPMC2168154 | biostudies-literature | 2007 Dec

REPOSITORIES: biostudies-literature

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CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila.

Herbert Erin E EE Cowles Kimberly N KN Goodrich-Blair Heidi H

Applied and environmental microbiology 20071019 24

The CpxRA signal transduction system, which in Escherichia coli regulates surface structure assembly and envelope maintenance, is involved in the pathogenic and mutualistic interactions of the entomopathogenic bacterium Xenorhabdus nematophila. When DeltacpxR1 cells were injected into Manduca sexta insects, the time required to kill 50% of the insects was twofold longer than the time observed for wild-type cells and the DeltacpxR1 cells ultimately killed 16% fewer insects than wild-type cells ki ...[more]

PMID: 17951441

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Project description:Xenorhabdus nematophila bacteria are mutualistic symbionts of Steinernema carpocapsae nematodes and pathogens of insects. The X. nematophila global regulator Lrp controls the expression of many genes involved in both mutualism and pathogenic activities, suggesting a role in the transition between the two host organisms. We previously reported that natural populations of X. nematophila exhibit various levels of Lrp expression and that cells expressing relatively low levels of Lrp are optimized for virulence in the insect Manduca sexta The adaptive advantage of the high-Lrp-expressing state was not established. Here we used strains engineered to express constitutively high or low levels of Lrp to test the model in which high-Lrp-expressing cells are adapted for mutualistic activities with the nematode host. We demonstrate that high-Lrp cells form more robust biofilms in laboratory media than do low-Lrp cells, which may reflect adherence to host tissues. Also, our data showed that nematodes cultivated with high-Lrp strains are more frequently colonized than are those associated with low-Lrp strains. Taken together, these data support the idea that high-Lrp cells have an advantage in tissue adherence and colonization initiation. Furthermore, our data show that high-Lrp-expressing strains better support nematode reproduction than do their low-Lrp counterparts under both in vitro and in vivo conditions. Our data indicate that heterogeneity of Lrp expression in X. nematophila populations provides diverse cell populations adapted to both pathogenic (low-Lrp) and mutualistic (high-Lrp) states.IMPORTANCE Host-associated bacteria experience fluctuating conditions during both residence within an individual host and transmission between hosts. For bacteria that engage in evolutionarily stable, long-term relationships with particular hosts, these fluctuations provide selective pressure for the emergence of adaptive regulatory mechanisms. Here we present evidence that the bacterium Xenorhabdus nematophila uses various levels of the transcription factor Lrp to optimize its association with its two animal hosts, nematodes and insects, with which it behaves as a mutualist and a pathogen, respectively. Building on our previous finding that relatively low cellular levels of Lrp are optimal for pathogenesis, we demonstrate that, conversely, high levels of Lrp promote mutualistic activities with the Steinernema carpocapsae nematode host. These data suggest that X. nematophila has evolved to utilize phenotypic variation between high- and low-Lrp-expression states to optimize its alternating behaviors as a mutualist and a pathogen.

Dataset Information

CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila.

Publications

CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila.

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