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Regulating alternative lifestyles in entomopathogenic bacteria.

ABSTRACT: Bacteria belonging to the genera Photorhabdus and Xenorhabdus participate in a trilateral symbiosis in which they enable their nematode hosts to parasitize insect larvae. The bacteria switch from persisting peacefully in a nematode's digestive tract to a lifestyle in which pathways to produce insecticidal toxins, degrading enzymes to digest the insect for consumption, and antibiotics to ward off bacterial and fungal competitors are activated. This study addresses three questions: (1) What molecular signal triggers antibiotic production in the bacteria? (2) What small molecules are regulated by the signal? And (3), how do the bacteria recognize the signal? Differential metabolomic profiling in Photorhabdus luminescens TT01 and Xenorhabdus nematophila revealed that L-proline in the insect's hemolymph initiates a metabolic shift. Small molecules known to be crucial for virulence and antibiosis in addition to previously unknown metabolites are dramatically upregulated by L-proline, linking the recognition of host environment to bacterial metabolic regulation. To identify the L-proline-induced signaling pathway, we deleted the proline transporters putP and proU in P. luminescens TT01. Studies of these strains support a model in which acquisition of L-proline both regulates the metabolic shift and maintains the bacterial proton motive force that ultimately regulates the downstream bacterial pathways affecting virulence and antibiotic production.

SUBMITTER: Crawford JM

PROVIDER: S-EPMC2821981 | biostudies-literature | 2010 Jan

REPOSITORIES: biostudies-literature

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Regulating alternative lifestyles in entomopathogenic bacteria.

Crawford Jason M JM Kontnik Renee R Clardy Jon J

Current biology : CB 20100101 1

Bacteria belonging to the genera Photorhabdus and Xenorhabdus participate in a trilateral symbiosis in which they enable their nematode hosts to parasitize insect larvae. The bacteria switch from persisting peacefully in a nematode's digestive tract to a lifestyle in which pathways to produce insecticidal toxins, degrading enzymes to digest the insect for consumption, and antibiotics to ward off bacterial and fungal competitors are activated. This study addresses three questions: (1) What molecu ...[more]

PMID: 20022247

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Project description:Temperature plays an important role in bacteria-host interactions and can be a determining factor for host switching. In this study we sought to investigate the reasons behind growth temperature restriction in the entomopathogenic enterobacterium Photorhabdus. Photorhabdus has a complex dual symbiotic and pathogenic life cycle. The genus consists of 19 species but only one subgroup, previously all classed together as Photorhabdus asymbiotica, have been shown to cause human disease. These clinical isolates necessarily need to be able to grow at 37°C, whilst the remaining species are largely restricted to growth temperatures below 34°C and are therefore unable to infect mammalian hosts. Here, we have isolated spontaneous mutant lines of Photorhabdus laumondii DJC that were able to grow up to 36-37°C. Following whole genome sequencing of 29 of these mutants we identified a single gene, encoding a protein with a RecG-like helicase domain that for the majority of isolates contained single nucleotide polymorphisms. Importantly, provision of the wild-type allele of this gene in trans restored the temperature restriction, confirming the mutations are recessive, and the dominant effect of the protein product of this gene. The gene appears to be part of a short three cistron operon, which we have termed the Temperature Restricting Locus (TRL). Transcription reporter strains revealed that this operon is induced upon the switch from 30 to 36°C, leading to replication arrest of the bacteria. TRL is absent from all of the human pathogenic species so far examined, although its presence is not uniform in different strains of the Photorhabdus luminescens subgroup. In a wider context, the presence of this gene is not limited to Photorhabdus, being found in phylogenetically diverse proteobacteria. We therefore suggest that this system may play a more fundamental role in temperature restriction in diverse species, relating to as yet cryptic aspects of their ecological niches and life cycle requirements.

Dataset Information

Regulating alternative lifestyles in entomopathogenic bacteria.

Publications

Regulating alternative lifestyles in entomopathogenic bacteria.

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