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  • Review Article
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Friend and foe: the two faces of Xenorhabdus nematophila

Key Points

  • The Gram-negative bacterium Xenorhabdus nematophila is a mutualist of a specific nematode species and a pathogen of insects, and is used as a model to study microorganism–host interactions and the similarities and differences underlying these symbioses.

  • The initial encounter between X. nematophila and its hosts is hypothesized to require nutrient and surface sensing by bacterial regulators, in addition to synthesis of bacterial effector proteins that can be delivered to host cells by outer membrane vesicles.

  • X. nematophila can survive and cause disease within insects by suppressing both cellular and humoral insect immunity. X. nematophila can suppress transcription of insect genes encoding antimicrobial peptides. X. nematophila also kills insect blood cells (haemocytes).

  • X. nematophila has an extensive array of virulence factors, including toxins, haemolysins, proteases, lipases and fimbriae.

  • In common with other mutualistic relationships between microorganisms and invertebrate hosts, the mutually beneficial relationship between X. nematophila and Steinernema carpocapsae nematodes involves nutrient exchange. Analysis of metabolic mutants suggests that the nematode might provide necessary nutrients to X. nematophila during growth within the nematode.

  • Transcriptional regulators of X. nematophila that contribute to virulence and mutualism have been described. These might function to sense the external environment and alter transcription of various surface and secreted proteins in response to these environmental stimuli.

Abstract

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 γ−proteobacterium Xenorhabdus nematophila. X. nematophila inhabits and influences the lives of two host animals, helping one to reproduce optimally while killing the other.

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Figure 1: Xenorhabdus nematophila in the infective juvenile stage of Steinernema carpocapsae.
Figure 2: The Xenorhabdus nematophila lifecycle.
Figure 3: Xenorhabdus nematophila putative effectors of host interactions.
Figure 4: Xenorhabdus nematophila colonization of Steinernema carpocapsae nematodes.
Figure 5: Xenorhabdus nematophila regulatory hierarchies control host interactions.

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Acknowledgements

Research on Xenorhabdus nematophila–host interactions is supported by the National Institutes of Health, the National Science Foundation and an Investigators in Pathogenesis of Infectious Disease Award from the Burroughs Wellcome Foundation. The authors are grateful to J. Chaston and E. Martens for supplying micrograph images.

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DATABASES

Entrez Genome Project

Bacillus anthracis

Bacillus thuringiensis

Borrelia burgdorferi

Caenorhabditis elegans

Campylobacter jejuni

Drosophila melanogaster

Escherichia coli

Haemophilus influenzae

Neisseria meningitidis

Photorhabdus luminescens

Proteus mirabilis

Salmonella enterica

Vibrio fischeri

Xenorhabdus bovienii

Xenorhabdus nematophila

Yersina pestis

Entrez Protein

EnvZ

LrhA

Lrp

MrxA

NilB

NilR

OmpR

PixA

FURTHER INFORMATION

Heidi Goodrich-Blair's homepage

Xenorhabdus nematophila genome

UW-Madison Symbiosis Cluster

Glossary

Mutualistic association

A long-term association between two or more organisms resulting in mutual benefit.

Pathogenic association

An interaction between two or more organisms that results in disease and/or death in one organism.

Vector

An animal that carries a microorganism from one place to another, generally between hosts or between a reservoir and a host.

Symbiosis

A long-term interaction between two or more organisms of different species that can be beneficial or harmful to one or more of the organisms.

Mucus

A substance that is secreted by an organism and contains glycoproteins. It is often used to collect, or protect, symbiotic microorganisms.

Cuticle

A non-cellular hardened outer casing of invertebrates.

Innate immunity

Immunity that is naturally present and generally non-specific; not dependent on prior exposure to antigens.

Axenic

An organism that is raised under sterile conditions, and is therefore devoid of bacteria.

Outer membrane vesicle

A double-membrane sphere that blebs off from a bacterial cell surface and can deliver virulence determinants or other microbial proteins to host cells.

Lectin

A glycan (carbohydrate)-binding protein.

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Herbert, E., Goodrich-Blair, H. Friend and foe: the two faces of Xenorhabdus nematophila. Nat Rev Microbiol 5, 634–646 (2007). https://doi.org/10.1038/nrmicro1706

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