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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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Figures

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  • Supplemental Material
  • FIG 1
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    FIG 1

    Experimental infection of the natural host of Arthroderma benhamiae. Cutaneously infected guinea pigs developed skin symptoms that were the most severe at 14 days postinfection (dpi) due to inflammation, while 8 dpi was the time point for the peak of infection.

  • FIG 2
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    FIG 2

    Prediction and manual correction of the gene coding for the autophagy protein Atg27 (ARB_01857; a transmembrane protein). (A) Original gene prediction; (B) automatic prediction from Augustus (signal peptide is missing); (C) final (new) gene prediction after manual correction. The reannotation of this particular gene is remarkable, as it produced a new intron, an alternative stop codon, and a manually corrected start codon.

  • FIG 3
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    FIG 3

    Characterization of the secretome. (A) Pie chart showing the main functional groups identified within the 457 proteins of the secretome. See detailed description in Data Set S1 in the supplemental material. (B) Pie charts showing the same functional groups as in panel A but within the 100 most expressed genes in Gp8 (in vivo 8 days postinfection), K (in vitro in keratin medium), and S (in vitro in soy medium). (C) Venn diagram of proteases (top) and carbohydrate/cell wall metabolism proteins (bottom) present in the 100 most expressed secreted proteins under the 3 conditions described for panel B. Proteases represent about 20% of the 100 most expressed proteins under the 3 conditions; however, the batch of proteins in Gp8 is clearly different from those in K and S. This trend is not as significant when comparing carbohydrate/cell wall metabolism proteins.

  • FIG 4
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    FIG 4

    Hierarchical clustering (A and C) and principal component (PC) analysis (B and D) of RNA sequencing samples considering the genes from the complete genome (A and B) or only the secretome subset (C and D). The sample names reflect the growth conditions: Cb, in vivo in guinea pig; S, in vitro in soy medium; Sa, in vitro in Sabouraud medium; K, in vitro in keratin medium. The in vivo samples cluster together.

  • FIG 5
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    FIG 5

    Number of differentially expressed genes versus the enumeration of all possible contrasting conditions in the genome and the secretome, using a cutoff of 1e−3 for FDR and 2 for the fold change.

  • FIG 6
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    FIG 6

    (A) The twenty-five most highly expressed genes encoding secreted proteins during infection compared to in vitro expression. (B) The twenty-five most highly expressed genes encoding secreted proteins in vitro (keratin medium) compared to in vivo expression. Abbreviations are as defined in the Fig. 4 legend.

Tables

  • Figures
  • Supplemental Material
  • TABLE 1

    RNA-seq data summarya

    LibraryTotal no. of cleaned reads (M)Reads aligned with organism:
    A. benhamiaeCavia porcellus
    No. of reads%No. of reads (M)%
    8 dpi34.50.5 M1.531.892.3
    31.71 M3.328.991.0
    261 M423.590.6
    14 dpi31.844.5 K0.13094.3
    30.651.2 K0.228.994.4
    31.424.8 K0.129.593.8
    27 dpi33.8623031.693.5
    39657036.694.0
    30.8452028.893.3
    44 dpi35.7458033.192.9
    31.9857029.692.7
    25.3808023.592.8
    Control26.1637024.393.4
    38.9840036.393.3
    35.73,143033.293.0
    Keratin12.46.1 M49.2
    13.57.9 M58.3
    13.98 M57.6
    Soy11.77.3 M62.6
    10.56 M57.1
    12.87.5 M58.8
    Sabouraud12.47.9 M63.5
    14.88.7 M59.1
    11.67.2 M61.6
    • ↵a M, million; K, thousand; dpi, days postinfection.

  • TABLE 2

    Comparison of new gene set and original onea

    New versus old gene predictionGene count in complete genomeGene count in secretome only
    With GPI Without GPI
    AutoManualAutoManual
    Matched2,66247 (13)2 (2)155 (55)0
    Alternative1,24619 (6)049 (19)1
    Different2,75231 (6)183 (19)10 (4)
    Merged2865 (2)07 (2)1
    Split761 (1)05 (2)0
    New3836034 (8)0
    Total7,405109 (28)3 (2)333 (105)12 (4)
    • ↵a Matched, identical old and new gene annotations; alternative, conserved start and stop codons but different splicing; different, different start or stop codons, possibly different splicing; merged, more than one old gene merged into a single new one; split, old gene split into several new ones; new, genes found only in the new predictions (708 original genes were lost); auto, gene annotations as produced by Augustus; manual, manual correction of the start codon. The number of genes whose products were confirmed by mass spectrometry in culture supernatants is given in parentheses. GPI, glycosylphosphatidylinositol.

  • TABLE 3

    Designation of samples and growth conditions

    RNA sampleGrowth condition
    CodeDescription
    Cb1Gp8 In vivo: guinea pig 8 days postinfection
    Cb2
    Cb3
    Cb4Gp14 In vivo: guinea pig 14 days postinfection
    Cb5
    Cb6
    K1K In vitro: keratin medium
    K2
    K3
    S1S In vitro: soy medium
    S2
    S4
    Sa1Sa In vitro: Sabouraud medium
    Sa2
    Sa3

Supplemental Material

  • Figures
  • Tables
  • Table S1

    The secretome: predicted cell surface/secreted proteins, putative functions, and expression. 1Open reading frame (ORF) names in this study. 2The status indicates the changes between previous proteome annotation and our prediction. 3ORF names in the previous genome annotation (Burmester et al., 2011). 4Names attributed to some proteases by Burmester et al. (2011) and Sriranganadane et al. (2011). 5UniProt accession numbers corresponding to the previous prediction. When two ORFs have been merged in the new prediction and both are present in UniProtKB, the two corresponding ACs are indicated. 6The presence of a signal peptide is indicated by SIG. SIG+GPI indicates that the gene product is predicted to have a GPI anchor. 7Mass spectrometry data were extracted from the work of Sriranganadane et al. (2011). For each identified gene product, we indicate the medium pH in which it was detected (either pH 4 or 7). 8Function has been assigned based on homology search in well-characterized fungi and/or from InterPro scanning to identify specific domains and families. Green identifies proteins with a potential role in proteolytic activity; red, proteins involved in carbohydrate metabolism; and orange, proteins involved in lipid metabolism. 9Homologous fungal allergens extracted from the Allergome database (http://www.allergome.org/ ). 10Name of weighted gene correlation network analysis (WGCNA) gene coexpression module. 11Summary of differential gene expression in vivo versus in vitro. Cutoffs: FDR = 1e−3 and 2-fold change. 12Significant expression trends from RNA sequencing data are indicated. The cutoff of −1 for the Z-score of transcripts per million was applied. 13Mean expression values expressed in transcripts per million for every growth condition. The detailed counts per sample are given in Table S3. Download Table S1, XLSX file, 0.1 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Data Set S1

    Supplemental materials and results. Download Data Set S1, PDF file, 0.2 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Table S2

    Potential allergens based on sequence homology. 1Open reading frame (ORF) names in this study that have homologs acting as allergens in other fungi (and wasp in the case of ARB_02861). 2Allergens were retrieved from the Allergome database (http://www.allergome.org/ ). 3The (+) indicates A. benhamiae allergen homologs identified as encoding putative cell surface/secreted proteins in our study. 4Function has been assigned based on homology search in well-characterized fungi and/or from InterPro scanning to identify specific domains and families. Download Table S2, XLSX file, 0.1 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Figure S1

    Manual curation on SUB10 and SED3. Actual and previous open reading frame predictions for SUB10 (A) and SED3 (B). N-terminal signal peptides, propeptides, and peptidase domains are illustrated with boxes of different hues. The corrections of assembly errors in actual open reading frames are indicated in red. Full ORFs were restored by the manual addition of the missing T in the SUB10 DNA sequence and G in the SED3 DNA sequence. These corrections have been confirmed by Sanger resequencing. The actual protein sequences of SUB10 and SED3 are available on the UniProtKB database (http://www.uniprot.org/ ) with respective accession numbers D4AQG0 and D4AK75 . Download Figure S1, PDF file, 0.1 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Table S3

    Detailed counts per sample, differential expression, and weighted gene correlation network analysis module attribution. Download Table S3, XLSX file, 1.4 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Figure S2

    Module-contrast correlations. Download Figure S2, PDF file, 0.1 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Figure S3

    Heat map of the turquoise module (A), blue module (B), tan module (C), midnight blue module (D), and yellow module (E). Download Figure S3, PDF file, 1.1 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Table S4

    Pathway enrichment analysis of weighted gene correlation network analysis modules. Only the most significant gene ontology terms are reported. Download Table S4, XLSX file, 0.1 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Figure S4

    The twelve most highly expressed genes encoding secreted proteases during infection (left table) and during in vitro growth in keratin medium (right table). Download Figure S4, PDF file, 0.1 MB.

    Copyright © 2016 Tran et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • Figure S5

    Quality of RNA extracted using the Qiagen RNA extraction kit (A) and the protocol described in Materials and Methods (B). The 18S rRNA and 28S rRNA absorbance peaks are shown in purple and blue, respectively. Download Figure S5, PDF file, 0.4 MB.

    Copyright © 2016 Tran et al.

    This content is 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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    • ABSTRACT
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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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