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The Bordetellae: lessons from genomics

Key Points

  • Preston, Parkhill and Maskell discuss the multiple, different aspects of Bordetella biology and show how the information gained from the recent completion of the comparative sequencing of three different Bordetella strains (Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica) has advanced our understanding of these fascinating bacteria. Specifically, these species are important models for studying how closely related bacteria have evolved different host ranges and the ability to cause different diseases in their hosts.

  • Genome structure, evolution and speciation are discussed, with specific mention of insertion elements and their role in genome evolution and the set of unique genes that have been identified for each Bordetella species.

  • Numerous factors that are involved in Bordetella virulence have been described. The authors discuss the insights that have been gained from genomic studies for specific factors and highlight new areas for future research.

  • Adhesins are important for infection, and Bordetella adhesins include the fhaB genes, and two newly described putative adhesins, fhaS, which is predicted to be similar to fhaB, and fhaL, which seems to be more divergent.

  • The complement of fimbrial genes found in each species that have been examined indicates that each species expresses different fimbriae types — although it is unlikely that fimbriae alone determine host adaptation.

  • Type IV pilus biogenesis in the bordetellae is restricted to B. bronchispetica and the authors present an examination of the type IV pili genes in detail. Type III secretion systems are also analysed.

  • Pertussis toxin has long been associated with B. pertussis pathogenesis, and the toxin was thought not to be expressed by B. parapertussis and B. bronchiseptica. Examination of the genome sequences shows that the toxin genes are indeed present in all three species, but challenges the current conception that B. parapertussis and B. bronchiseptica have acquired promoter-silencing mutations, prompting new evaluation of the contribution of pertussis toxin to Bordetella pathogenesis.

  • What determines the host adaptation and restriction of these species? The authors consider several factors including the metabolic repertoire of the species as a determining factor.

Abstract

Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica are very closely related, but have different host ranges and cause different diseases in their hosts. The Bordetella genome project, which sequenced the genomes of representative strains of these three important pathogens concurrently, has recently been completed. This comparative genomics resource will be of immense value to researchers investigating the basis of host specificity and speciation in bacteria. Here, we draw together key aspects of Bordetella biology and highlight the new findings that have been uncovered by this project.

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Figure 1: Diagram depicting the rearrangements in, and deletions from, the genomes of B. pertussis and B. parapertussis compared with B. bronchiseptica.
Figure 2: A schematic diagram that depicts the action of the Bvg two-component system.
Figure 3: Repeat motifs in FhaL.
Figure 4: Alignment of the amino-terminal amino acid sequences of the putative major pilin or minor pilin subunits of the B. bronchiseptica tfp locus.

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Acknowledgements

Work in the laboratory of D.J.M is funded by a Wellcome Trust Programme Grant. Work in the laboratory of A.J.P. is funded by the Canadian Bacterial Diseases Network (CBDN).

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DATABASES

Entrez

Bordetella bronchiseptica

Bordetella parapertussis

Bordetella pertussis

Haemophilus influenzae

Helicobacter pylori

Mycobacterium tuberculosis

Salmonella enterica serovar Typhi

Salmonella enterica serovar Typhimurium

Streptococcus pyogenes

Yersinia pestis

SwissProt

BvgA

BvgS

FhaB

FhaL

FhaS

FimA

Fim2

Fim3

The Protein Data Bank

pertussis toxin

FURTHER INFORMATION

B. avium genome sequence project

Glossary

POLYMORPHISMS

The existence within a species or population of different forms of individuals. In the context of this review, genetic polymorphisms refer to the existence of multiple alleles at a gene locus.

SPECIATION

The evolution of new species.

PSEUDOGENE

A DNA sequence that is related to a functional gene but which has accumulated mutations that prevent expression of a functional product.

GENOMOTYPING

The typing of strains by genome-wide analysis. This is often accomplished by the use of DNA microarrays, and is greatly facilitated by the generation of genome sequences.

SLIP-STRAND MISPAIRING

Tandem direct repeats might incorrectly pair during DNA replication. For example, 'slippage' between template and newly synthesized DNA strands during replication might result in pairing between, for example, the third repeat unit on the new strand and the fourth repeat on the template strand. Such mispairing results in a change in the number of repeats in the newly synthesized strand compared with the template DNA.

SIDEROPHORE

A compound that chelates iron.

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Preston, A., Parkhill, J. & Maskell, D. The Bordetellae: lessons from genomics. Nat Rev Microbiol 2, 379–390 (2004). https://doi.org/10.1038/nrmicro886

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