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Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi

Anke Burmester12, Ekaterina Shelest3, Gernot Glöckner4, Christoph Heddergott12, Susann Schindler56, Peter Staib7, Andrew Heidel4, Marius Felder48, Andreas Petzold4, Karol Szafranski4, Marc Feuermann9, Ivo Pedruzzi9, Steffen Priebe3, Marco Groth4, Robert Winkler106, Wenjun Li11, Olaf Kniemeyer1, Volker Schroeckh1, Christian Hertweck106, Bernhard Hube126, Theodore C White13, Matthias Platzer4, Reinhard Guthke3, Joseph Heitman11, Johannes Wöstemeyer2, Peter F Zipfel56, Michel Monod14 and Axel A Brakhage12*

Author Affiliations

1 Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Beutenbergstrasse 11a, Jena, 07745, Germany

2 Institute of Microbiology, Friedrich Schiller University (FSU) Jena, Neugasse 24, Jena, 07743, Germany

3 Systems Biology/Bioinformatics group, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Beutenbergstrasse 11a, Jena, 07745, Germany

4 Genome Analysis group, Leibniz Institute for Age Research - Fritz Lipmann Institute (FLI), Beutenbergstrasse 11, Jena, 07745, Germany

5 Department of Infection Biology, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Beutenbergstrasse 11a, Jena, 07745, Germany

6 Friedrich Schiller University (FSU) Jena, Fürstengraben 26, Jena, 07743, Germany

7 Junior Research Group Fundamental Molecular Biology of Pathogenic Fungi, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Beutenbergstrasse 11a, Jena, 07745, Germany

8 Biocomputing group, Leibniz Institute for Age Research - Fritz Lipmann Institute (FLI), Beutenbergstrasse 11, Jena, 07745, Germany

9 Swiss-Prot group, SIB, Swiss Institute of Bioinformatics, 1 rue Michel Servet, Geneve, 1204, Switzerland

10 Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Beutenbergstrasse 11a, Jena, 07745, Germany

11 Department of Molecular Genetics and Microbiology, Duke University Medical Center, 322 CARL Building, Box 3546 DUMC, Durham, NC 27710, USA

12 Department of Microbial Pathogenicity Mechanisms, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Beutenbergstrasse 11a, Jena, 07745, Germany

13 Seattle Biomedical Research Institute, University of Washington, 307 Westlake Ave, N., Suite 500, Seattle, WA 98109-5219, USA

14 Department of Dermatology, Centre Hospitalier Universitaire Vaudois, Lausanne, CH-1011, Switzerland

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Genome Biology 2011, 12:R7  doi:10.1186/gb-2011-12-1-r7

Published: 19 January 2011

Abstract

Background

Millions of humans and animals suffer from superficial infections caused by a group of highly specialized filamentous fungi, the dermatophytes, which exclusively infect keratinized host structures. To provide broad insights into the molecular basis of the pathogenicity-associated traits, we report the first genome sequences of two closely phylogenetically related dermatophytes, Arthroderma benhamiae and Trichophyton verrucosum, both of which induce highly inflammatory infections in humans.

Results

97% of the 22.5 megabase genome sequences of A. benhamiae and T. verrucosum are unambiguously alignable and collinear. To unravel dermatophyte-specific virulence-associated traits, we compared sets of potentially pathogenicity-associated proteins, such as secreted proteases and enzymes involved in secondary metabolite production, with those of closely related onygenales (Coccidioides species) and the mould Aspergillus fumigatus. The comparisons revealed expansion of several gene families in dermatophytes and disclosed the peculiarities of the dermatophyte secondary metabolite gene sets. Secretion of proteases and other hydrolytic enzymes by A. benhamiae was proven experimentally by a global secretome analysis during keratin degradation. Molecular insights into the interaction of A. benhamiae with human keratinocytes were obtained for the first time by global transcriptome profiling. Given that A. benhamiae is able to undergo mating, a detailed comparison of the genomes further unraveled the genetic basis of sexual reproduction in this species.

Conclusions

Our results enlighten the genetic basis of fundamental and putatively virulence-related traits of dermatophytes, advancing future research on these medically important pathogens.