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Open Access Research article

The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae

Roy Gross1*, Carlos A Guzman2*, Mohammed Sebaihia3, Vítor AP Martins dos Santos4, Dietmar H Pieper5, Ralf Koebnik6, Melanie Lechner1, Daniela Bartels137, Jens Buhrmester148, Jomuna V Choudhuri157, Thomas Ebensen2, Lars Gaigalat8, Stefanie Herrmann9, Amit N Khachane4, Christof Larisch7, Stefanie Link1, Burkhard Linke7, Folker Meyer137, Sascha Mormann8, Diana Nakunst8, Christian Rückert8, Susanne Schneiker-Bekel7, Kai Schulze2, Frank-Jörg Vorhölter8, Tetyana Yevsa2, Jacquelyn T Engle10, William E Goldman11, Alfred Pühler8, Ulf B Göbel9, Alexander Goesmann7, Helmut Blöcker12, Olaf Kaiser147 and Rosa Martinez-Arias12

Author Affiliations

1 Chair of Microbiology, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany

2 Department of Vaccinology and Applied Microbiology, Helmholtz Center for Infection Research, D-38124 Braunschweig, Germany

3 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SA, UK

4 Division of Molecular Biotechnology, Helmholtz Center for Infection Research, D-38124 Braunschweig, Germany

5 Department of Microbial Pathogenesis, Helmholtz Center for Infection Research, D-38124 Braunschweig, Germany

6 Institut de Recherche pour le Développement UMR 5096, CNRS-UP-IRD 911, Avenue Agropolis, BP 64501, 34394 Montpellier, Cedex 5, France

7 Center for Biotechnology (CeBiTec), Bielefeld University, D-33501 Bielefeld, Germany

8 Chair of Genetics, Bielefeld University, D-33501 Bielefeld, Germany

9 Institute for Microbiology and Hygiene, Charité Berlin, Dorotheen-Str. 96, D-10117 Berlin, Germany

10 Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110, USA

11 Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, USA

12 Department of Genome Analysis, Helmholtz Center for Infection Research, D-38124 Braunschweig, Germany

13 Mathematics and Computer Science Division, Argonne National Laboratory, USA

14 Roche Diagnostics GmbH, Nonnenwald 2, D-82377 Penzberg, Germany

15 BASF Plant Science GmbH, D-67117 Limburgerhof, Germany

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BMC Genomics 2008, 9:449  doi:10.1186/1471-2164-9-449

Published: 30 September 2008

Abstract

Background

Bordetella petrii is the only environmental species hitherto found among the otherwise host-restricted and pathogenic members of the genus Bordetella. Phylogenetically, it connects the pathogenic Bordetellae and environmental bacteria of the genera Achromobacter and Alcaligenes, which are opportunistic pathogens. B. petrii strains have been isolated from very different environmental niches, including river sediment, polluted soil, marine sponges and a grass root. Recently, clinical isolates associated with bone degenerative disease or cystic fibrosis have also been described.

Results

In this manuscript we present the results of the analysis of the completely annotated genome sequence of the B. petrii strain DSMZ12804. B. petrii has a mosaic genome of 5,287,950 bp harboring numerous mobile genetic elements, including seven large genomic islands. Four of them are highly related to the clc element of Pseudomonas knackmussii B13, which encodes genes involved in the degradation of aromatics. Though being an environmental isolate, the sequenced B. petrii strain also encodes proteins related to virulence factors of the pathogenic Bordetellae, including the filamentous hemagglutinin, which is a major colonization factor of B. pertussis, and the master virulence regulator BvgAS. However, it lacks all known toxins of the pathogenic Bordetellae.

Conclusion

The genomic analysis suggests that B. petrii represents an evolutionary link between free-living environmental bacteria and the host-restricted obligate pathogenic Bordetellae. Its remarkable metabolic versatility may enable B. petrii to thrive in very different ecological niches.