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Research Article | Host-Microbe Biology

RNA Sequencing-Based Genome Reannotation of the Dermatophyte Arthroderma benhamiae and Characterization of Its Secretome and Whole Gene Expression Profile during Infection

Van Du T. Tran, Niccolò De Coi, Marc Feuermann, Emanuel Schmid-Siegert, Elena-Tatiana Băguţ, Bernard Mignon, Patrice Waridel, Corinne Peter, Sylvain Pradervand, Marco Pagni, Michel Monod
Barbara Methe, Editor
Van Du T. Tran
aVital-IT group, SIB Swiss Institute of Bioinformatics, Lausanne, Switzerland
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  • ORCID record for Van Du T. Tran
Niccolò De Coi
bDepartment of Dermatology, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
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Marc Feuermann
cSwiss-Prot Group, SIB Swiss Institute of Bioinformatics, Geneva, Switzerland
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Emanuel Schmid-Siegert
aVital-IT group, SIB Swiss Institute of Bioinformatics, Lausanne, Switzerland
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Elena-Tatiana Băguţ
dFundamental and Applied Research for Animals & Health (FARAH), Department of Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium
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Bernard Mignon
dFundamental and Applied Research for Animals & Health (FARAH), Department of Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium
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Patrice Waridel
eProtein Analysis Facility, Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland
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Corinne Peter
fGenomic Technologies Facility, Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland
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Sylvain Pradervand
fGenomic Technologies Facility, Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland
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Marco Pagni
aVital-IT group, SIB Swiss Institute of Bioinformatics, Lausanne, Switzerland
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Michel Monod
bDepartment of Dermatology, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
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Barbara Methe
University of Pittsburgh
Roles: Editor
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DOI: 10.1128/mSystems.00036-16
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ABSTRACT

Dermatophytoses (ringworm, jock itch, athlete’s foot, and nail infections) are the most common fungal infections, but their virulence mechanisms are poorly understood. Combining transcriptomic data obtained from growth under various culture conditions with data obtained during infection led to a significantly improved genome annotation. About 65% of the protein-encoding genes predicted with our protocol did not match the existing annotation for A. benhamiae. Comparing gene expression during infection on guinea pigs with keratin degradation in vitro, which is supposed to mimic the host environment, revealed the critical importance of using real in vivo conditions for investigating virulence mechanisms. The analysis of genes expressed in vivo, encoding cell surface and secreted proteins, particularly proteases, led to the identification of new allergen and virulence factor candidates. Dermatophytes are the most common agents of superficial mycoses in humans and animals. The aim of the present investigation was to systematically identify the extracellular, possibly secreted, proteins that are putative virulence factors and antigenic molecules of dermatophytes. A complete gene expression profile of Arthroderma benhamiae was obtained during infection of its natural host (guinea pig) using RNA sequencing (RNA-seq) technology. This profile was completed with those of the fungus cultivated in vitro in two media containing either keratin or soy meal protein as the sole source of nitrogen and in Sabouraud medium. More than 60% of transcripts deduced from RNA-seq data differ from those previously deposited for A. benhamiae. Using these RNA-seq data along with an automatic gene annotation procedure, followed by manual curation, we produced a new annotation of the A. benhamiae genome. This annotation comprised 7,405 coding sequences (CDSs), among which only 2,662 were identical to the currently available annotation, 383 were newly identified, and 15 secreted proteins were manually corrected. The expression profile of genes encoding proteins with a signal peptide in infected guinea pigs was found to be very different from that during in vitro growth when using keratin as the substrate. Especially, the sets of the 12 most highly expressed genes encoding proteases with a signal sequence had only the putative vacuolar aspartic protease gene PEP2 in common, during infection and in keratin medium. The most upregulated gene encoding a secreted protease during infection was that encoding subtilisin SUB6, which is a known major allergen in the related dermatophyte Trichophyton rubrum. IMPORTANCE Dermatophytoses (ringworm, jock itch, athlete’s foot, and nail infections) are the most common fungal infections, but their virulence mechanisms are poorly understood. Combining transcriptomic data obtained from growth under various culture conditions with data obtained during infection led to a significantly improved genome annotation. About 65% of the protein-encoding genes predicted with our protocol did not match the existing annotation for A. benhamiae. Comparing gene expression during infection on guinea pigs with keratin degradation in vitro, which is supposed to mimic the host environment, revealed the critical importance of using real in vivo conditions for investigating virulence mechanisms. The analysis of genes expressed in vivo, encoding cell surface and secreted proteins, particularly proteases, led to the identification of new allergen and virulence factor candidates.

  • Copyright © 2016 Tran et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license .

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RNA Sequencing-Based Genome Reannotation of the Dermatophyte Arthroderma benhamiae and Characterization of Its Secretome and Whole Gene Expression Profile during Infection
Van Du T. Tran, Niccolò De Coi, Marc Feuermann, Emanuel Schmid-Siegert, Elena-Tatiana Băguţ, Bernard Mignon, Patrice Waridel, Corinne Peter, Sylvain Pradervand, Marco Pagni, Michel Monod
mSystems Aug 2016, 1 (4) e00036-16; DOI: 10.1128/mSystems.00036-16

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RNA Sequencing-Based Genome Reannotation of the Dermatophyte Arthroderma benhamiae and Characterization of Its Secretome and Whole Gene Expression Profile during Infection
Van Du T. Tran, Niccolò De Coi, Marc Feuermann, Emanuel Schmid-Siegert, Elena-Tatiana Băguţ, Bernard Mignon, Patrice Waridel, Corinne Peter, Sylvain Pradervand, Marco Pagni, Michel Monod
mSystems Aug 2016, 1 (4) e00036-16; DOI: 10.1128/mSystems.00036-16
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KEYWORDS

NO MESH TERMS ASSIGNED AS OF 10-11-2019
Arthroderma benhamiae
RNA-seq
Trichophyton
annotation
dermatophytes
infection
proteases
secreted proteins

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