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Invertebrates as a source of emerging human pathogens

Nature Reviews Microbiology volume 2, pages 833–841 (2004)Cite this article

Abstract

Despite their importance, little is known about the origins of many emerging human pathogens. However, given the age and current predominance of invertebrates, it is likely that bacteria—invertebrate interactions are not only a present source of human pathogens but have also shaped their evolution. Pathogens of invertebrate and unicellular organisms represent an extensive reservoir of bacterial strains equipped with virulence factors that evolved to overcome the innate immune responses of their hosts. This reservoir might represent a source of new human pathogenic strains and might also foster the spread of novel virulence factors into existing human commensal or pathogenic bacteria. This article examines the available evidence for this concept by examining pairs of closely related bacteria, one of which is benign, but insect associated, and one of which is a human pathogen.

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Figure 1: Evolution of the virulence gene pool.
Figure 2: Common themes in insect and mammalian immunity.
Figure 3: Pathogenicity islands encode both insect and mammalian virulence factors.
Figure 4: Making the leap from invertebrates to vertebrates.

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Acknowledgements

We thank various reviewers for helpful comments and ideas in the preparation of this manuscript. Work in our laboratories is funded by the BBSRC, the Wellcome Trust, the Medical Research Council and the DSTL.

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Authors and Affiliations

  1. Department of Biology and Biochemistry, Centre for Molecular Microbiology, University of Bath, Bath, BA2 7AY, UK

    Nicholas R. Waterfield & Richard H. ffrench-Constant

  2. Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT, UK

    Brendan W. Wren

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DATABASES

Entrez

Bacillus anthracis

Bacillus cereus

Bacillus thuringiensis

Caenorhabditis elegans

pADAP

Photorhabdus luminescens

Pseudomonas fluorescens

Pseudomonas syringae

tcaC/tcdB

tccC

Yersinia enterocolitica

Yersinia pestis

Y. pestis CO92 strain

Y. pestis KIM10 strain

FURTHER INFORMATION

Photorhabdus asymbiotica

Yersinia pseudotuberculosis

Wellcome Trust Sanger Institute

Glossary

CHITINASE

The outer skeleton of invertebrates is hardened with chitin. As invertebrates are so numerous on both land and sea, one of the most common enzymes used by bacteria are the chitinases — enzymes that degrade chitin.

ENTOMOPATHOGENIC

Pathogenic to insects.

HAEMOCOEL

In contrast to vertebrates, invertebrate blood systems are open sacs (haemocoels), within which phagocytic cells (haemocytes) are found.

MELANIN ENCAPSULATION PROCESS

As well as being used to clot blood, the melanisation reaction can also be used to trap foreign invaders such as bacteria, which are wrapped in layers of haemocytes and trapped in a melanised capsule to isolate them from the rest of the haemocoel.

PHENOL-OXIDASE

Similar to the human clotting reaction, insects use the melanisation reaction to clot the blood. The final clot is composed of melanin and the final step of the process is mediated by cleavage of the inactive pro-phenyloxidase to the active phenol-oxidase.

SHORT-RANGE SYNTENY

Conservation in the order of gene homologues on the chromosome.

SYMBIONT

Symbiosis and pathogenicity can be viewed as two extremes of one contiuum of interaction between bacteria and their hosts. Photorhabdus spp. are termed obligate pathogens as their life cycle indicates that they must kill the insect host to be taken up again by the nematode vector (and symbiont).

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Waterfield, N., Wren, B. & ffrench-Constant, R. Invertebrates as a source of emerging human pathogens. Nat Rev Microbiol 2, 833–841 (2004). https://doi.org/10.1038/nrmicro1008

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