Genome sequencing and comparative genomics analysis revealed pathogenic potential in Penicillium capsulatum as a novel fungal pathogen belonging to Eurotiales

Frontiers in Microbiology

Volumn 7, Issue OCT, 2016, Pages

  Yang, Ying ^a,b,c   Chen, Min ^d,e,f   Li, Zongwei ^g   Al Hatmi, Abdullah M S ^e,f,h   de Hoog, Sybren ^e,f   Pan, Weihua ^d   Ye, Qiang ^c,i   Bo, Xiaochen ^b   Li, Zhen ^b   Wang, Shengqi ^b   Wang, Junzhi ^c   Chen, Huipeng ^a   Liao, Wanqing ^d  

^a BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

^b BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^c NATIONAL INSTITUTES FOR FOOD AND DRUG CONTROL   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

^e CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

^g Center for Hospital Infection Control   (China)

^h MINISTRY OF HEALTH   (Oman)

ⁱ BEIJING HOSPITAL   (China)

Author keywords

Comparative genomics; Genome sequencing; Novel fungal pathogen; Penicillium capsulatum

Indexed keywords

GENOMIC DNA;

ARTICLE; EUROTIALES; FUNGAL VIRULENCE; FUNGUS ISOLATION; GENE CLUSTER; GENE SEQUENCE; HOST PARASITE INTERACTION; NONHUMAN; PENICILLIUM; PENICILLIUM CAPSULATUM; PHYLOGENOMICS; PHYLOGENY; RNA EXTRACTION;

EID: 84996931915     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01541     Document Type: Article

References (73)

1. Abad, A., Fernandez-Molina, J. V., Bikandi, J., Ramirez, A., Margareto, J., Sendino, J., et al. (2010). What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev. Iberoam. Micol. 27, 155-182. doi: 10.1016/j.riam.2010.10.003
2. Al-Bader, N., Vanier, G., Liu, H., Gravelat, F. N., Urb, M., Hoareau, C. M., et al. (2010). Role of trehalose biosynthesis in Aspergillus fumigatus development, stress response, and virulence. Infect. Immun. 78, 3007-3018. doi: 10.1128/IAI.00813-09
3. Amich, J., Vicentefranqueira, R., Leal, F., and Calera, J. A. (2010). Aspergillus fumigatus survival in alkaline and extreme zinc-limiting environments relies on the induction of a zinc homeostasis system encoded by the zrfC and aspf2 genes. Eukaryot. Cell 9, 424-437. doi: 10.1128/EC.00348-09
4. Bhabhra, R., Miley, M. D., Mylonakis, E., Boettner, D., Fortwendel, J., Panepinto, J. C., et al. (2004). Disruption of the Aspergillus fumigatus gene encoding nucleolar protein CgrA impairs thermotolerant growth and reduces virulence. Infect. Immun. 72, 4731-4740. doi: 10.1128/IAI.72.8.4731-4740.2004
5. Blin, K., Medema, M. H., Kazempour, D., Fischbach, M. A., Breitling, R., Takano, E., et al. (2013). antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 41, W204-W212. doi: 10.1093/nar/gkt449
6. Brakhage, A. A., and Liebmann, B. (2005). Aspergillus fumigatus conidial pigment and cAMP signal transduction: significance for virulence. Med. Mycol. 43(Suppl. 1), S75-S82. doi: 10.1080/13693780400028967
7. Brown, J. S., Aufauvre-Brown, A., Brown, J., Jennings, J. M., Arst, H. Jr., and Holden, D. W. (2000). Signature-tagged and directed mutagenesis identify PABA synthetase as essential for Aspergillus fumigatus pathogenicity. Mol. Microbiol. 36, 1371-1380. doi: 10.1046/j.1365-2958.2000.01953.x
8. Calera, J. A., Paris, S., Monod, M., Hamilton, A. J., Debeaupuis, J. P., Diaquin, M., et al. (1997). Cloning and disruption of the antigenic catalase gene of Aspergillus fumigatus. Infect. Immun. 65, 4718-4724.
9. Chabane, S., Sarfati, J., Ibrahim-Granet, O., Du, C., Schmidt, C., Mouyna, I., et al. (2006). Glycosylphosphatidylinositol-anchored Ecm33p influences conidial cell wall biosynthesis in Aspergillus fumigatus. Appl. Environ. Microbiol. 72, 3259-3267. doi: 10.1128/AEM.72.5.3259-3267.2006
10. Chakrabarti, A., and Slavin, M. A. (2011). Endemic fungal infections in the Asia-Pacific region. Med. Mycol. 49, 337-344. doi: 10.3109/13693786.2010.551426
11. Chen, K. H., Miadlikowska, J., Molnar, K., Arnold, A. E., U'Ren, J. M., Gaya, E., et al. (2015). Phylogenetic analyses of eurotiomycetous endophytes reveal their close affinities to Chaetothyriales, Eurotiales, and a new order-Phaeomoniellales. Mol. Phylogenet. Evol. 85, 117-130. doi: 10.1016/j.ympev.2015.01.008
12. Chen, M., Houbraken, J., Pan, W., Zhang, C., Peng, H., Wu, L., et al. (2013). Pulmonary fungus ball caused by Penicillium capsulatum in a patient with type 2 diabetes: a case report. BMC Infect. Dis. 13:496. doi: 10.1186/1471-2334-13-496
13. Clemons, K. V., Miller, T. K., Selitrennikoff, C. P., and Stevens, D. A. (2002). fos-1, a putative histidine kinase as a virulence factor for systemic aspergillosis. Med. Mycol. 40, 259-262. doi: 10.1080/714031112
14. Darling, A. E., Mau, B., and Perna, N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147. doi: 10.1371/journal.pone.0011147
15. Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164-1165. doi: 10.1093/bioinformatics/btr088
16. D'Enfert, C., Diaquin, M., Delit, A., Wuscher, N., Debeaupuis, J. P., Huerre, M., et al. (1996). Attenuated virulence of uridine-uracil auxotrophs of Aspergillus fumigatus. Infect. Immun. 64, 4401-4405.
17. Ferrarini, M., Moretto, M., Ward, J. A., Surbanovski, N., Stevanovic, V., Giongo, L., et al. (2013). An evaluation of the PacBio RS platform for sequencing and de novo assembly of a chloroplast genome. BMC Genomics 14:670. doi: 10.1186/1471-2164-14-670
18. Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., et al. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-194. doi: 10.1038/nature10947
19. Garcia-Solache, M. A., and Casadevall, A. (2010). Global warming will bring new fungal diseases for mammals. MBio 1:e00061-10. doi: 10.1128/mBio.00061-10
20. Gastebois, A., Clavaud, C., Aimanianda, V., and Latge, J. P. (2009). Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Future Microbiol. 4, 583-595. doi: 10.2217/Fmb.09.29
21. Hissen, A. H., Wan, A. N., Warwas, M. L., Pinto, L. J., and Moore, M. M. (2005). The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N5-oxygenase, is required for virulence. Infect. Immun. 73, 5493-5503. doi: 10.1128/iai.73.9.5493-5503.2005
22. Houbraken, J., and Samson, R. A. (2011). Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Stud. Mycol. 70, 1-51. doi: 10.3114/sim.2011.70.01
23. Jaton-Ogay, K., Paris, S., Huerre, M., Quadroni, M., Falchetto, R., Togni, G., et al. (1994). Cloning and disruption of the gene encoding an extracellular metalloprotease of Aspergillus fumigatus. Mol. Microbiol. 14, 917-928. doi: 10.1111/j.1365-2958.1994.tb01327.x
24. Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L., et al. (2008). Global trends in emerging infectious diseases. Nature 451, 990-993. doi: 10.1038/nature06536
25. Jones, P., Binns, D., Chang, H. Y., Fraser, M., Li, W., McAnulla, C., et al. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236-1240. doi: 10.1093/bioinformatics/btu031
26. Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O., and Walichiewicz, J. (2005). Repbase update, a database of eukaryotic repetitive elements. Cytogenet. Genome. Res. 110, 462-467. doi: 10.1159/000084979
27. Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. doi: 10.1093/molbev/mst010
28. Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., et al. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647-652. doi: 10.1038/nature09575
29. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., and Salzberg, S. L. (2013). TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36. doi: 10.1186/gb-2013-14-4-r36
30. Kolattukudy, P. E., Lee, J. D., Rogers, L. M., Zimmerman, P., Ceselski, S., Fox, B., et al. (1993). Evidence for possible involvement of an elastolytic serine protease in aspergillosis. Infect. Immun. 61, 2357-2368.
31. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., et al. (2009). Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645. doi: 10.1101/gr.092759.109
32. Kurtz, S., Phillippy, A., Delcher, A. L., Smoot, M., Shumway, M., Antonescu, C., et al. (2004). Versatile and open software for comparing large genomes. Genome Biol. 5:R12. doi: 10.1186/gb-2004-5-2-r12
33. Langfelder, K., Jahn, B., Gehringer, H., Schmidt, A., Wanner, G., and Brakhage, A. A. (1998). Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med. Microbiol. Immunol. 187, 79-89. doi: 10.1007/s004300050077
34. Lavezzo, E., Toppo, S., Franchin, E., Di Camillo, B., Finotello, F., Falda, M., et al. (2013). Genomic comparative analysis and gene function prediction in infectious diseases: application to the investigation of a meningitis outbreak. BMC Infect. Dis. 13:554. doi: 10.1186/1471-2334-13-554
35. Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760. doi: 10.1093/bioinformatics/btp324
36. Li, H., and Durbin, R. (2010). Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595. doi: 10.1093/bioinformatics/btp698
37. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., et al. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079. doi: 10.1093/bioinformatics/btp352
38. Li, L., Stoeckert, C. J. Jr., and Roos, D. S. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189. doi: 10.1101/gr.1224503
39. Li, Y., Wang, Z. K., Liu, X., Song, Z. Y., Li, R., Shao, C. W., et al. (2016). Siderophore biosynthesis but not reductive iron assimilation is essential for the dimorphic fungus Nomuraea rileyi conidiation, dimorphism transition, resistance to oxidative stress, pigmented microsclerotium formation, and virulence. Front. Microbiol. 7:931. doi: 10.3389/fmicb.2016.00931
40. Lowe, T. M., and Eddy, S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964. doi: 10.1093/nar/25.5.0955
41. Lyratzopoulos, G., Ellis, M., Nerringer, R., and Denning, D. W. (2002). Invasive infection due to penicillium species other than P. marneffei. J Infect. 45, 184-195. doi: 10.1053/jinf.2002.1056
42. Maubon, D., Park, S., Tanguy, M., Huerre, M., Schmitt, C., Prevost, M. C., et al. (2006). AGS3, an alpha(1-3)glucan synthase gene family member of Aspergillus fumigatus, modulates mycelium growth in the lung of experimentally infected mice. Fungal Genet. Biol. 43, 366-375. doi: 10.1016/j.fgb.2006.01.006
43. May, G. S., Xue, T., Kontoyiannis, D. P., and Gustin, M. C. (2005). Mitogen activated protein kinases of Aspergillus fumigatus. Med. Mycol. 43(Suppl. 1), S83-S86. doi: 10.1080/13693780400024784
44. Moreno, M. A., Ibrahim-Granet, O., Vicentefranqueira, R., Amich, J., Ave, P., Leal, F., et al. (2007). The regulation of zinc homeostasis by the ZafA transcriptional activator is essential for Aspergillus fumigatus virulence. Mol. Microbiol. 64, 1182-1197. doi: 10.1111/j.1365-2958.2007.05726.x
45. Morens, D. M., Folkers, G. K., and Fauci, A. S. (2004). The challenge of emerging and re-emerging infectious diseases. Nature 430, 242-249. doi: 10.1038/nature02759
46. Mouyna, I., Fontaine, T., Vai, M., Monod, M., Fonzi, W. A., Diaquin, M., et al. (2000a). Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J. Biol. Chem. 275, 14882-14889. doi: 10.1074/jbc.275.20.14882
47. Mouyna, I., Henry, C., Doering, T. L., and Latge, J. P. (2004). Gene silencing with RNA interference in the human pathogenic fungus Aspergillus fumigatus. FEMS Microbiol. Lett. 237, 317-324. doi: 10.1016/j.femsle.2004.06.048
48. Mouyna, I., Monod, M., Fontaine, T., Henrissat, B., Lechenne, B., and Latge, J. P. (2000b). Identification of the catalytic residues of the first family of beta(1-3)glucanosyltransferases identified in fungi. Biochem. J. 347(Pt 3), 741-747. doi: 10.1042/bj3470741
49. Mouyna, I., Morelle, W., Vai, M., Monod, M., Lechenne, B., Fontaine, T., et al. (2005). Deletion of GEL2 encoding for a beta(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol. Microbiol. 56, 1675-1688. doi: 10.1111/j.1365-2958.2005.04654.x
50. Pareek, C. S., Smoczynski, R., and Tretyn, A. (2011). Sequencing technologies and genome sequencing. J. Appl. Genet. 52, 413-435. doi: 10.1007/s13353-011-0057-x
51. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786. doi: 10.1038/nmeth.1701
52. Pitt, J. I. (1994). The current role of Aspergillus and Penicillium in human and animal health. J. Med. Vet. Mycol. 32(Suppl. 1), 17-32. doi: 10.1080/02681219480000701
53. Pott, G. B., Miller, T. K., Bartlett, J. A., Palas, J. S., and Selitrennikoff, C. P. (2000). The isolation of FOS-1, a gene encoding a putative two-component histidine kinase from Aspergillus fumigatus. Fungal Genet. Biol. 31, 55-67. doi: 10.1006/fgbi.2000.1225
54. Reeves, E. P., Reiber, K., Neville, C., Scheibner, O., Kavanagh, K., and Doyle, S. (2006). A nonribosomal peptide synthetase (Pes1) confers protection against oxidative stress in Aspergillus fumigatus. FEBS J. 273, 3038-3053. doi: 10.1111/j.1742-4658.2006.05315.x
55. Reichard, U., Buttner, S., Eiffert, H., Staib, F., and Ruchel, R. (1990). Purification and characterisation of an extracellular serine proteinase from Aspergillus fumigatus and its detection in tissue. J. Med. Microbiol. 33, 243-251. doi: 10.1099/00222615-33-4-243
56. Romano, J., Nimrod, G., Ben-Tal, N., Shadkchan, Y., Baruch, K., Sharon, H., et al. (2006). Disruption of the Aspergillus fumigatus ECM33 homologue results in rapid conidial germination, antifungal resistance and hypervirulence. Microbiology 152(Pt 7), 1919-1928. doi: 10.1099/mic.0.28936-0
57. Samson, R. A., Visagie, C. M., Houbraken, J., Hong, S. B., Hubka, V., Klaassen, C. H., et al. (2014). Phylogeny, identification and nomenclature of the genus Aspergillus. Stud. Mycol. 78, 141-173. doi: 10.1016/j.simyco.2014.07.004
58. Samson, R. A., Yilmaz, N., Houbraken, J., Spierenburg, H., Seifert, K. A., Peterson, S. W., et al. (2011). Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated in Penicillium subgenus Biverticillium. Stud. Mycol. 70, 159-183. doi: 10.3114/sim.2011.70.04
59. Schattner, P., Brooks, A. N., and Lowe, T. M. (2005). The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33, W686-W689. doi: 10.1093/nar/gki366
60. Schrettl, M., Bignell, E., Kragl, C., Sabiha, Y., Loss, O., Eisendle, M., et al. (2007). Distinct roles for intra-and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog. 3:e128. doi: 10.1371/journal.ppat.0030128
61. Sheppard, D. C., and Filler, S. G. (2015). Host cell invasion by medically important fungi. Cold Spring Harb. Perspect. Med. 5:a019687. doi: 10.1101/cshperspect.a019687
62. Sonnhammer, E. L., von Heijne, G., and Krogh, A. (1998). A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6, 175-182.
63. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313. doi: 10.1093/bioinformatics/btu033
64. Stanke, M., Diekhans, M., Baertsch, R., and Haussler, D. (2008). Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24, 637-644. doi: 10.1093/bioinformatics/btn013
65. Steinbach, W. J., Cramer, R. A. Jr., Perfect, B. Z., Asfaw, Y. G., Sauer, T. C., Najvar, L. K., et al. (2006). Calcineurin controls growth, morphology, and pathogenicity in Aspergillus fumigatus. Eukaryot. Cell 5, 1091-1103. doi: 10.1128/EC.00139-06
66. Steinbach, W. J., Cramer, R. A. Jr., Perfect, B. Z., Henn, C., Nielsen, K., Heitman, J., et al. (2007). Calcineurin inhibition or mutation enhances cell wall inhibitors against Aspergillus fumigatus. Antimicrob. Agents Chemother. 51, 2979-2981. doi: 10.1128/AAC.01394-06
67. Struelens, M. J., and Brisse, S. (2013). From molecular to genomic epidemiology: transforming surveillance and control of infectious diseases. Euro. Surveill. 18:20386.
68. Tang, C. M., Cohen, J., Krausz, T., Van Noorden, S., and Holden, D. W. (1993). The alkaline protease of Aspergillus fumigatus is not a virulence determinant in two murine models of invasive pulmonary aspergillosis. Infect. Immun. 61, 1650-1656.
69. Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., et al. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515. doi: 10.1038/nbt.1621
70. Tsitsigiannis, D. I., Bok, J. W., Andes, D., Nielsen, K. F., Frisvad, J. C., and Keller, N. P. (2005). Aspergillus cyclooxygenase-like enzymes are associated with prostaglandin production and virulence. Infect. Immun. 73, 4548-4559. doi: 10.1128/IAI.73.8.4548-4559.2005
71. Urban, M., Pant, R., Raghunath, A., Irvine, A. G., Pedro, H., and Hammond-Kosack, K. E. (2015). The pathogen-host interactions database (PHI-base): additions and future developments. Nucleic Acids Res. 43, D645-D655. doi: 10.1093/nar/gku1165
72. van den Berg, M. A., Albang, R., Albermann, K., Badger, J. H., Daran, J. M., Driessen, A. J., et al. (2008). Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26, 1161-1168. doi: 10.1038/nbt.1498
73. Wagener, J., Echtenacher, B., Rohde, M., Kotz, A., Krappmann, S., Heesemann, J., et al. (2008). The putative alpha-1,2-mannosyltransferase AfMnt1 of the opportunistic fungal pathogen Aspergillus fumigatus is required for cell wall stability and full virulence. Eukaryot. Cell 7, 1661-1673. doi: 10.1128/Ec.00221-08