1887

Microbial Genomics logo

Volume 6, Issue 10

Transcriptome-wide expression profiling of yeast and mycelial forms and the establishment of the Sporothrix Genome DataBase Open Access

Abstract

is a dimorphic fungus existing as mould in the environment and as yeast in the host. The morphological shift between mycelial/yeast phases is crucial for its virulence, but the transcriptional networks implicated in dimorphic transition are still not fully understood. Here, we report the global transcriptomic differences occurring between mould and yeast phases of , including changes in gene expression profiles associated with these distinct cellular phenotypes. Moreover, we also propose a new genome annotation, which reveals a more complex transcriptional architecture than previously assumed. Using RNA-seq, we identified a total of 17 307 genes, of which 11 217 were classified as protein-encoding genes, whereas 6090 were designated as non-coding RNAs (ncRNAs). Approximately ~71 % of all annotated genes were found to overlap and the different-strand overlapping type was the most common. Gene expression analysis revealed that 8795 genes were differentially regulated among yeast and mould forms. Differential gene expression was also observed for antisense ncRNAs overlapping neighbouring protein-encoding genes. The release of transcriptome-wide data and the establishment of the Sporothrix Genome DataBase (http://sporothrixgenomedatabase.unime.it) represent an important milestone for research, because they provide a strong basis for future studies on the molecular pathways involved in numerous biological processes.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): gene expression , long non-coding RNAs , overlapping genes , RNA-seq , Sporothrix schenckii and sporotrichosis
Funding
This study was supported by the:
  • Sun Yat-sen University (Award 82000-31143405)
    • Principle Award Recipient: Huaiqiu Huang
  • National Nature Foundation of China (Award 81371746 and 81974300)
    • Principle Award Recipient: Huaiqiu Huang
  • Ministero dell’Istruzione, dell’Università e della Ricerca (Award FFABRA2017)
    • Principle Award Recipient: Giuseppe Criseo
  • Università degli Studi di Messina (Award CT_ROMEO_GOM grant agreement n° 36036)
    • Principle Award Recipient: Orazio Romeo
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000445
2020-10-09
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/10/mgen000445.html?itemId=/content/journal/mgen/10.1099/mgen.0.000445&mimeType=html&fmt=ahah

References

  1. de Beer ZW, Duong TA, Wingfield MJ. The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol 2016; 83:165–191 [View Article][PubMed]
     [Google Scholar]
  2. Rodrigues AM, Della Terra PP, Gremião ID, Pereira SA, Orofino-Costa R et al. The threat of emerging and re-emerging pathogenic Sporothrix species. Mycopathologia 2020 [View Article][PubMed]
     [Google Scholar]
  3. Ramírez-Soto MC, Aguilar-Ancori EG, Tirado-Sánchez A, Bonifaz A. Ecological determinants of sporotrichosis etiological agents. J Fungi 2018; 4:95 [View Article][PubMed]
     [Google Scholar]
  4. Arenas R, Sánchez-Cardenas CD, Ramirez-Hobak L, Ruíz Arriaga LF, Vega Memije ME. Sporotrichosis: from KOH to molecular biology. J Fungi 2018; 4:62 [View Article][PubMed]
     [Google Scholar]
  5. Chakrabarti A, Bonifaz A, Gutierrez-Galhardo MC, Mochizuki T, Li S. Global epidemiology of sporotrichosis. Med Mycol 2015; 53:3–14 [View Article][PubMed]
     [Google Scholar]
  6. Mora-Montes HM, Dantas Ada S, Trujillo-Esquivel E, de Souza Baptista AR, Lopes-Bezerra LM. Current progress in the biology of members of the Sporothrix schenckii complex following the genomic era. FEMS Yeast Res 2015; 15:fov065 [View Article][PubMed]
     [Google Scholar]
  7. Téllez MD, Batista-Duharte A, Portuondo D, Quinello C, Bonne-Hernández R et al. Sporothrix schenckii complex biology: environment and fungal pathogenicity. Microbiology 2014; 160:2352–2365 [View Article][PubMed]
     [Google Scholar]
  8. Marimon R, Serena C, Gené J, Cano J, Guarro J. In vitro antifungal susceptibilities of five species of Sporothrix . Antimicrob Agents Chemother 2008; 52:732–734 [View Article][PubMed]
     [Google Scholar]
  9. Arrillaga-Moncrieff I, Capilla J, Mayayo E, Marimon R, Mariné M et al. Different virulence levels of the species of Sporothrix in a murine model. Clin Microbiol Infect 2009; 15:651–655 [View Article][PubMed]
     [Google Scholar]
  10. Castro RA, Kubitschek-Barreira PH, Teixeira PAC, Sanches GF, Teixeira MM et al. Differences in cell morphometry, cell wall topography and gp70 expression correlate with the virulence of Sporothrix brasiliensis clinical isolates. PLoS One 2013; 8:e75656 [View Article][PubMed]
     [Google Scholar]
  11. Zhang Y, Hagen F, Stielow B, Rodrigues AM, Samerpitak K et al. Phylogeography and evolutionary patterns in Sporothrix spanning more than 14 000 human and animal case reports. Persoonia 2015; 35:1–20 [View Article][PubMed]
     [Google Scholar]
  12. Batista-Duharte A, Téllez-Martínez D, Roberto de Andrade C, Portuondo DL, Jellmayer JA et al. Sporothrix brasiliensis induces a more severe disease associated with sustained Th17 and regulatory T cells responses than Sporothrix schenckii sensu stricto in mice. Fungal Biol 2018; 122:1163–1170 [View Article][PubMed]
     [Google Scholar]
  13. Teixeira MM, de Almeida LGP, Kubitschek-Barreira P, Alves FL, Kioshima ES et al. Comparative genomics of the major fungal agents of human and animal sporotrichosis: Sporothrix schenckii and Sporothrix brasiliensis . BMC Genomics 2014; 15:943 [View Article][PubMed]
     [Google Scholar]
  14. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
     [Google Scholar]
  15. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013; 29:15–21 [View Article][PubMed]
     [Google Scholar]
  16. Okonechnikov K, Conesa A, García-Alcalde F. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 2016; 32:292–294 [View Article][PubMed]
     [Google Scholar]
  17. Campbell MS, Holt C, Moore B, Yandell M. Genome annotation and curation using MAKER and MAKER-P. Curr Protoc Bioinformatics 2014; 48:4.11.1–4.11.39 [View Article][PubMed]
     [Google Scholar]
  18. Korf I. Gene finding in novel genomes. BMC Bioinformatics 2004; 5:59 [View Article][PubMed]
     [Google Scholar]
  19. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 2005; 33:W465–W467 [View Article][PubMed]
     [Google Scholar]
  20. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011; 29:644–652 [View Article][PubMed]
     [Google Scholar]
  21. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012; 28:3150–3152 [View Article][PubMed]
     [Google Scholar]
  22. Gremme G, Steinbiss S, Kurtz S. GenomeTools: a comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans Comput Biol Bioinform 2013; 10:645–656 [View Article][PubMed]
     [Google Scholar]
  23. Boratyn GM, Camacho C, Cooper PS, Coulouris G, Fong A et al. BLAST: a more efficient report with usability improvements. Nucleic Acids Res 2013; 41:W29–W33 [View Article][PubMed]
     [Google Scholar]
  24. Jones P, Binns D, Chang HY, Fraser M, Li W et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014; 30:1236–1240 [View Article][PubMed]
     [Google Scholar]
  25. Kang YJ, Yang DC, Kong L, Hou M, Meng YQ et al. CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features. Nucleic Acids Res 2017; 45:W12–W16 [View Article][PubMed]
     [Google Scholar]
  26. Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 2013; 29:2933–2935 [View Article][PubMed]
     [Google Scholar]
  27. Chan PP, Lowe TM. tRNAscan-SE: searching for tRNA genes in genomic sequences. Methods Mol Biol 2019; 1962:1–14 [View Article][PubMed]
     [Google Scholar]
  28. Törönen P, Medlar A, Holm L. PANNZER2: a rapid functional annotation web server. Nucleic Acids Res 2018; 46:W84–W88 [View Article][PubMed]
     [Google Scholar]
  29. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article][PubMed]
     [Google Scholar]
  30. Sanna CR, Li WH, Zhang L. Overlapping genes in the human and mouse genomes. BMC Genomics 2008; 9:169 [View Article][PubMed]
     [Google Scholar]
  31. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014; 30:923–930 [View Article][PubMed]
     [Google Scholar]
  32. Donaldson ME, Ostrowski LA, Goulet KM, Saville BJ. Transcriptome analysis of smut fungi reveals widespread intergenic transcription and conserved antisense transcript expression. BMC Genomics 2017; 18:340 [View Article][PubMed]
     [Google Scholar]
  33. Rau A, Gallopin M, Celeux G, Jaffrézic F. Data-based filtering for replicated high-throughput transcriptome sequencing experiments. Bioinformatics 2013; 29:2146–2152 [View Article][PubMed]
     [Google Scholar]
  34. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139–140 [View Article][PubMed]
     [Google Scholar]
  35. Tian T, Liu Y, Yan H, You Q, Yi X et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 2017; 45:W122–W129 [View Article]
     [Google Scholar]
  36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 2001; 25:402–408 [View Article][PubMed]
     [Google Scholar]
  37. Buels R, Yao E, Diesh CM, Hayes RD, Munoz-Torres M et al. JBrowse: a dynamic web platform for genome visualization and analysis. Genome Biol 2016; 17:66 [View Article][PubMed]
     [Google Scholar]
  38. Kahl G. The Dictionary of Genomics, Transcriptomics and Proteomics, 5th edn. Weinheim: Wiley-VCH; 2015
     [Google Scholar]
  39. Wood EJ, Chin-Inmanu K, Jia H, Lipovich L. Sense-antisense gene pairs: sequence, transcription, and structure are not conserved between human and mouse. Front Genet 2013; 4:183 [View Article][PubMed]
     [Google Scholar]
  40. Donaldson ME, Saville BJ. Natural antisense transcripts in fungi. Mol Microbiol 2012; 85:405–417 [View Article][PubMed]
     [Google Scholar]
  41. Atkinson SR, Marguerat S, Bitton DA, Rodríguez-López M, Rallis C et al. Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast. RNA 2018; 24:1195–1213 [View Article][PubMed]
     [Google Scholar]
  42. Han G, Cheng C, Zheng Y, Wang X, Xu Y et al. Identification of long non-coding RNAs and the regulatory network responsive to arbuscular mycorrhizal fungi colonization in maize roots. Int J Mol Sci 2019; 20:4491 [View Article][PubMed]
     [Google Scholar]
  43. Borgognone A, Sanseverino W, Aiese Cigliano R, Castanera R. Distribution, characteristics, and regulatory potential of long noncoding RNAs in brown-rot fungi. Int J Genomics 2019; 2019:9702342 [View Article][PubMed]
     [Google Scholar]
  44. Fernandes JCR, Acuña SM, Aoki JI, Floeter-Winter LM, Muxel SM. Long non-coding RNAs in the regulation of gene expression: physiology and disease. Noncoding RNA 2019; 5:17 [View Article]
     [Google Scholar]
  45. Linde J, Duggan S, Weber M, Horn F, Sieber P et al. Defining the transcriptomic landscape of Candida glabrata by RNA-Seq. Nucleic Acids Res 2015; 43:1392–1406 [View Article][PubMed]
     [Google Scholar]
  46. Cemel IA, Ha N, Schermann G, Yonekawa S, Brunner M. The coding and noncoding transcriptome of Neurospora crassa . BMC Genomics 2017; 18:978 [View Article][PubMed]
     [Google Scholar]
  47. Guo R, Chen DF, Xiong CL, Hou CS, Zheng YZ et al. First identification of long non-coding RNAs in fungal parasite Nosema ceranae . Apidologie 2018; 49:660–670 [View Article]
     [Google Scholar]
  48. Latgé G, Poulet C, Bours V, Josse C, Jerusalem G. Natural antisense transcripts: molecular mechanisms and implications in breast cancers. Int J Mol Sci 2018; 19:123 [View Article][PubMed]
     [Google Scholar]
  49. Chen C-H, Pan C-Y, Lin W. Overlapping protein-coding genes in human genome and their coincidental expression in tissues. Sci Rep 2019; 9:13377 [View Article][PubMed]
     [Google Scholar]
  50. Sabath N, Graur D, Landan G. Same-strand overlapping genes in bacteria: compositional determinants of phase bias. Biol Direct 2008; 3:36 [View Article][PubMed]
     [Google Scholar]
  51. Harris KA, Breaker RR. Large noncoding RNAs in bacteria. Microbiol Spectr 2018; 6:RWR-0005-2017 [View Article][PubMed]
     [Google Scholar]
  52. Gong X, Fu Y, Jiang D, Li G, Yi X et al. L-Arginine is essential for conidiation in the filamentous fungus Coniothyrium minitans . Fungal Genet Biol 2007; 44:1368–1379 [View Article][PubMed]
     [Google Scholar]
  53. Cánovas D, Marcos JF, Marcos AT, Strauss J. Nitric oxide in fungi: is there NO light at the end of the tunnel?. Curr Genet 2016; 62:513–518 [View Article][PubMed]
     [Google Scholar]
  54. Liu X, Cai Y, Zhang X, Zhang H, Zheng X et al. Carbamoyl phosphate synthetase subunit MoCpa2 affects development and pathogenicity by modulating arginine biosynthesis in Magnaporthe oryzae . Front Microbiol 2016; 7:2023 [View Article][PubMed]
     [Google Scholar]
  55. Han T-L, Cannon RD, Gallo SM, Villas-Bôas SG. A metabolomic study of the effect of Candida albicans glutamate dehydrogenase deletion on growth and morphogenesis. NPJ Biofilms Microbiomes 2019; 5:13 [View Article]
     [Google Scholar]
  56. Hou B, Zhang Z, Zheng F, Liu X. Molecular cloning, characterization and differential expression of DRK1 in Sporothrix schenckii . Int J Mol Med 2013; 31:99–104 [View Article][PubMed]
     [Google Scholar]
  57. Zhang Z, Hou B, Wu YZ, Wang Y, Liu X et al. Two‑component histidine kinase DRK1 is required for pathogenesis in Sporothrix schenckii . Mol Med Rep 2018; 17:721–728 [View Article][PubMed]
     [Google Scholar]
  58. Defosse TA, Sharma A, Mondal AK, Dugé de Bernonville T, Latgé J-P et al. Hybrid histidine kinases in pathogenic fungi. Mol Microbiol 2015; 95:914–924 [View Article][PubMed]
     [Google Scholar]
  59. Pathan EK, Ghormade V, Panmei R, Deshpande MV. Biochemical and molecular aspects of dimorphism in fungi. In Satyanarayana T, Deshmukh S, Deshpande M. eds Advancing Frontiers in Mycology and Mycotechnology Singapore: Springer; 2019 pp 69–94
     [Google Scholar]
  60. Chacko N, Zhao Y, Yang E, Wang L, Cai JJ et al. The lncRNA RZE1 controls cryptococcal morphological transition. PLoS Genet 2015; 11:e1005692 [View Article][PubMed]
     [Google Scholar]
  61. Till P, Mach RL, Mach-Aigner AR. A current view on long noncoding RNAs in yeast and filamentous fungi. Appl Microbiol Biotechnol 2018; 102:7319–7331 [View Article][PubMed]
     [Google Scholar]
  62. Wang Z, Jiang Y, Wu H, Xie X, Huang B. Genome-wide identification and functional prediction of long non-coding RNAs involved in the heat stress response in Metarhizium robertsii . Front Microbiol 2019; 10:2336 [View Article][PubMed]
     [Google Scholar]
  63. D'Alessandro E, Giosa D, Huang L, Zhang J, Gao W et al. Draft genome sequence of the dimorphic fungus Sporothrix pallida, a nonpathogenic species belonging to Sporothrix, a genus containing agents of human and feline sporotrichosis. Genome Announc 2016; 4:e00184-16 [View Article][PubMed]
     [Google Scholar]
  64. Huang L, Gao W, Giosa D, Criseo G, Zhang J et al. Whole-genome sequencing and in silico analysis of two strains of Sporothrix globosa . Genome Biol Evol 2016; 8:3292–3296 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000445
Loading
Transcriptome-wide expression profiling of Sporothrix schenckii yeast and mycelial forms and the establishment of the Sporothrix Genome DataBase
M Gen 6, e000445 (2020); https://doi.org/10.1099/mgen.0.000445
/content/journal/mgen/10.1099/mgen.0.000445
/content/journal/mgen/10.1099/mgen.0.000445
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error