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  • Review Article
  • Published:

The tad locus: postcards from the widespread colonization island

Nature Reviews Microbiology volume 5, pages 363–375 (2007)Cite this article

Key Points

  • The tad (tight adherence) locus was initially identified in the periodontal pathogen Aggregatibacter (Actinobacillus) actinomycetemcomitans and the aquatic bacterium Caulobacter crescentus.

  • The tad genes encode a macromolecular transport system that is required for biogenesis of Flp (fimbrial low-molecular-weight protein) pili. Bundles of Flp pili, called fibrils, are produced by clinical isolates of A. actinomycetemcomitans and are required for tenacious biofilm formation and pathogenesis.

  • Homologues of tad genes are present in all sequenced Archaea and in many, but not all, Gram-negative and Gram-positive bacteria.

  • We suggest that type II macromolecular transport should be defined by the ancient primary association between the TadA and TadB/C homologues (for example, GspE and GspF). The Tad secretion system, along with all archaeal tad-like loci, would represent one major subtype of type II secretion, while the other major subtype would contain classical type II secretion and type IV pilus systems.

  • Some Tad proteins are homologous to components of bacterial type II or type IV secretion systems, but almost all of the tad genes comprise early branching, anciently diverged lineages. For instance, the Flp proteins belong to a distinct subfamily of type IVb prepilins.

  • Several Tad proteins (such as RcpC, RcpB, TadZ, TadD, TadE, TadF and TadG) seem to be unique to the Tad macromolecular transport system.

  • There is accumulating evidence to show that tad loci are important for colonization and/or pathogenesis of a number of bacterial species, including A. actinomycetemcomitans, Aggregatibacter (Haemophilus) aphrophilus, C. crescentus, Haemophilus ducreyi, Pasteurella multocida, Pseudomonas aeruginosa, Yersinia ruckeri and Burkholderia pseudomallei.

  • The functions of individual Tad proteins, as well as their interactions within the Tad apparatus, are just beginning to be dissected. Future studies of the Tad macromolecular transport system will undoubtedly reveal its unique features, as well as further illuminate prokaryotic protein secretion in general.

Abstract

The Tad (tight adherence) macromolecular transport system, which is present in many bacterial and archaeal species, represents an ancient and major new subtype of type II secretion. The tad genes are present on a genomic island named the widespread colonization island (WCI), and encode the machinery that is required for the assembly of adhesive Flp (fimbrial low-molecular-weight protein) pili. The tad genes are essential for biofilm formation, colonization and pathogenesis in the genera Aggregatibacter (Actinobacillus), Haemophilus, Pasteurella, Pseudomonas, Yersinia, Caulobacter and perhaps others. Here we review the structure, function and evolution of the Tad secretion system.

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Figure 1: Physical maps of tad loci from Gram-negative bacteria, Actinobacteria and Archaea.
Figure 2: Phylogenetic tree of bacterial and archaeal secretion NTPases.
Figure 3: Flp fibrils from Aggregatibacter (Actinobacillus) actinomycetemcomitans.
Figure 4: Hypothetical structure and function of the Tad secretion system.

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Acknowledgements

The authors would like to thank all members of the Figurski laboratory, and particularly B. Perez, S. Clock and V. Weaver Grosso, for helpful discussions that greatly strengthened this manuscript. We are deeply indebted to D. Fine and R. DeSalle for their considerable help and encouragement. We are also grateful to Y. Puius for assistance with electron microscopy, and to J. Boddey for sharing unpublished results. D.H.F. is particularly grateful to S. Silverstein and A. Mitchell for their support. This work was supported by grants to D.H.F. and to R. DeSalle and D.H.F. from the US National Institutes of Health.

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Author notes

  1. Mladen Tomich and Paul J. Planet: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Microbiology, College of Physicians and Surgeons, Columbia University, 701 West 168th Street, New York, 10032, USA

    Mladen Tomich & David H. Figurski

  2. American Museum of Natural History, Molecular Laboratories, Central Park West at 79th Street, New York, 10024, USA

    Paul J. Planet

  3. Department of Pediatrics, Children's Hospital of New York, 630 west 168th Street, New York, 10032, USA

    Paul J. Planet

Authors
  1. Mladen Tomich
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  2. Paul J. Planet
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  3. David H. Figurski
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Corresponding author

Correspondence to David H. Figurski.

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Supplementary information

Supplementary information S1

Phylogenetic tree of bacterial and archaeal secretion NTPases. (PDF 157 kb)

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DATABASES

Entrez Genome Project

Actinobacillus actinomycetemcomitans

Bordetella pertussis

Burkholderia pseudomallei

Caulobacter crescentus

Mesorhizobium loti

Mycobacterium tuberculosis

Neisseria gonorrhoeae

Neisseria meningitidis

Pseudomonas aeruginosa

Sinorhizobium meliloti

Vibrio cholerae

Vibrio vulnificus

Yersinia pestis

FURTHER INFORMATION

C. crescentus

Glossary

Genomic island

A mobile genetic element acquired by horizontal transfer, which carries multiple genes that are typically involved in pathogenesis or symbiosis.

Capnophilic

Bacterial species that grow best in the presence of elevated levels of carbon dioxide, relative to air.

Twitching motility

A flagellum-independent motility on solid surfaces exhibited by some Gram-negative bacteria, mediated by retraction of type IV pili.

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Tomich, M., Planet, P. & Figurski, D. The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 5, 363–375 (2007). https://doi.org/10.1038/nrmicro1636

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