Clade II Candida auris possess genomic structural variations related to an ancestral strain
Autoři:
Tsuyoshi Sekizuka aff001; Shigekazu Iguchi aff002; Takashi Umeyama aff003; Yuba Inamine aff001; Koichi Makimura aff004; Makoto Kuroda aff001; Yoshitsugu Miyazaki aff003; Ken Kikuchi aff002
Působiště autorů:
Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan
aff001; Department of Infectious Diseases, Tokyo Women’s Medical University, Tokyo, Japan
aff002; Department of Chemotherapy and Mycoses, National Institute of Infectious Diseases, Tokyo, Japan
aff003; Department of Medical Mycology, Graduate School of Medicine, Teikyo University, Tokyo, Japan
aff004
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223433
Souhrn
Candida auris is an invasive and multidrug-resistant ascomycetous yeast that is under global surveillance. All clinical cases of C. auris infection diagnosed from 1997 to 2019 in Japan were non-invasive and sporadic otitis media cases. In the present study, we performed whole-genome sequencing of seven C. auris strains isolated from patients with otitis media in Japan, all of which belonged to clade II. Comparative genome analysis using the high-quality draft genome sequences JCM 15448T revealed that single nucleotide variations (SNVs), clade-specific accessory genes, and copy number variations (CNVs) were identified in each C. auris clade. A total of 61 genes involved in cell wall and stress response-related functions was absent in clade II, and the pattern of conserved CNVs in each clade was more stable in clade II than in other clades. Our data suggest that the genomic structural diversity is stable in C. auris isolated from each biogeographic location, and Japanese strains isolated from patients with otitis media might belong to an ancestral type of C. auris. One Japanese strain, TWCC 58362, with reduced susceptibility to fluconazole, exhibited no mutation in ergosterol biosynthesis-related genes (ERG). However, TWCC 58362-specific variations, including SNVs, indels, and CNVs were detected, suggesting that gene duplication events in C. auris might contribute to antifungal drug resistance. Taken together, we demonstrated that genomic structural variations in C. auris could correlate to geographical dissemination, epidemiology, lesions in the host, and antifungal resistance.
Klíčová slova:
Comparative genomics – Phylogenetic analysis – Mitochondrial DNA – DNA sequence analysis – Sequence databases – Antimicrobial resistance – Copy number variation – Japan
Zdroje
1. Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, et al. First three reported cases of nosocomial fungemia caused by Candida auris. J Clin Microbiol. 2011;49: 3139–3142. doi: 10.1128/JCM.00319-11 21715586
2. Chowdhary A, Sharma C, Duggal S, Agarwal K, Prakash A, Singh PK, et al. New clonal strain of Candida auris, Delhi, India. Emerging Infect Dis. 2013;19: 1670–1673. doi: 10.3201/eid1910.130393 24048006
3. Sarma S, Kumar N, Sharma S, Govil D, Ali T, Mehta Y, et al. Candidemia caused by amphotericin B and fluconazole resistant Candida auris. Indian J Med Microbiol. 2013;31: 90–91. doi: 10.4103/0255-0857.108746 23508441
4. Chowdhary A, Anil Kumar V, Sharma C, Prakash A, Agarwal K, Babu R, et al. Multidrug-resistant endemic clonal strain of Candida auris in India. Eur J Clin Microbiol Infect Dis. 2014;33: 919–926. doi: 10.1007/s10096-013-2027-1 24357342
5. Magobo RE, Corcoran C, Seetharam S, Govender NP. Candida auris-associated candidemia, South Africa. Emerging Infect Dis. 2014;20: 1250–1251. doi: 10.3201/eid2007.131765 24963796
6. Calvo B, Melo ASA, Perozo-Mena A, Hernandez M, Francisco EC, Hagen F, et al. First report of Candida auris in America: Clinical and microbiological aspects of 18 episodes of candidemia. J Infect. 2016;73: 369–374. doi: 10.1016/j.jinf.2016.07.008 27452195
7. Borman AM, Szekely A, Johnson EM. Comparative Pathogenicity of United Kingdom Isolates of the Emerging Pathogen Candida auris and Other Key Pathogenic Candida Species. mSphere. 2016;1. doi: 10.1128/mSphere.00189-16 27547827
8. Borman AM, Szekely A, Johnson EM. Isolates of the emerging pathogen Candida auris present in the UK have several geographic origins. Med Mycol. 2017;55: 563–567. doi: 10.1093/mmy/myw147 28204557
9. Ben-Ami R, Berman J, Novikov A, Bash E, Shachor-Meyouhas Y, Zakin S, et al. Multidrug-Resistant Candida haemulonii and C. auris, Tel Aviv, Israel. Emerging Infect Dis. 2017;23. doi: 10.3201/eid2302.161486 28098529
10. Vallabhaneni S, Kallen A, Tsay S, Chow N, Welsh R, Kerins J, et al. Investigation of the First Seven Reported Cases of Candida auris, a Globally Emerging Invasive, Multidrug-Resistant Fungus-United States, May 2013-August 2016. Am J Transplant. 2017;17: 296–299. doi: 10.1111/ajt.14121 28029734
11. Morales-López SE, Parra-Giraldo CM, Ceballos-Garzón A, Martínez HP, Rodríguez GJ, Álvarez-Moreno CA, et al. Invasive Infections with Multidrug-Resistant Yeast Candida auris, Colombia. Emerging Infect Dis. 2017;23: 162–164. doi: 10.3201/eid2301.161497 27983941
12. Schelenz S, Hagen F, Rhodes JL, Abdolrasouli A, Chowdhary A, Hall A, et al. First hospital outbreak of the globally emerging Candida auris in a European hospital. Antimicrob Resist Infect Control. 2016;5: 35. doi: 10.1186/s13756-016-0132-5 27777756
13. Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A, Govender NP, et al. Simultaneous Emergence of Multidrug-Resistant Candida auris on 3 Continents Confirmed by Whole-Genome Sequencing and Epidemiological Analyses. Clin Infect Dis. 2017;64: 134–140. doi: 10.1093/cid/ciw691 27988485
14. Dominguez EG, Zarnowski R, Choy HL, Zhao M, Sanchez H, Nett JE, et al. Conserved Role for Biofilm Matrix Polysaccharides in Candida auris Drug Resistance. mSphere. 2019;4. doi: 10.1128/mSphereDirect.00680-18 30602527
15. Eyre DW, Sheppard AE, Madder H, Moir I, Moroney R, Quan TP, et al. A Candida auris Outbreak and Its Control in an Intensive Care Setting. N Engl J Med. 2018;379: 1322–1331. doi: 10.1056/NEJMoa1714373 30281988
16. Yamaguchi H, Uchida K, Nishiyama Y, Group TJASP. Species distribution and in vitro susceptibility to three antifungal triazoles of clinical Candida isolates from a five-year nation-wide survey in Japan. Medical Mycology Research. 2012;3: 17–26.
17. Ishikane M, Hayakawa K, Kutsuna S, Takeshita N, Ohmagari N. Epidemiology of Blood Stream Infection due to Candida Species in a Tertiary Care Hospital in Japan over 12 Years: Importance of Peripheral Line-Associated Candidemia. PLoS ONE. 2016;11: e0165346. doi: 10.1371/journal.pone.0165346 27798663
18. Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K, Yamaguchi H. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol Immunol. 2009;53: 41–44. doi: 10.1111/j.1348-0421.2008.00083.x 19161556
19. Iguchi S, Mizushima R, Kamada K, Itakura Y, Yoshida A, Uzawa Y, et al. The Second Candida auris Isolate from Aural Discharge in Japan. Jpn J Infect Dis. 2018;71: 174–175. doi: 10.7883/yoken.JJID.2017.466 29491246
20. Kim M-N, Shin JH, Sung H, Lee K, Kim E-C, Ryoo N, et al. Candida haemulonii and closely related species at 5 university hospitals in Korea: identification, antifungal susceptibility, and clinical features. Clin Infect Dis. 2009;48: e57–61. doi: 10.1086/597108 19193113
21. Kwon YJ, Shin JH, Byun SA, Choi MJ, Won EJ, Lee D, et al. Candida auris Clinical Isolates from South Korea: Identification, Antifungal Susceptibility, and Genotyping. Land GA, editor. J Clin Microbiol. American Society for Microbiology Journals; 2019;57: 3139. doi: 10.1128/JCM.01624-18 30728190
22. Iguchi S, Itakura Y, Yoshida A, Kamada K, Mizushima R, Arai Y, et al. Candida auris: A pathogen difficult to identify, treat, and eradicate and its characteristics in Japanese strains. J Infect Chemother. 2019;25: 743–749. doi: 10.1016/j.jiac.2019.05.034 31257156
23. Escandón P, Chow NA, Caceres DH, Gade L, Berkow EL, Armstrong P, et al. Molecular epidemiology of Candida auris in Colombia reveals a highly-related, country-wide colonization with regional patterns in Amphotericin B resistance. Clin Infect Dis. 2018. doi: 10.1093/cid/ciy411
24. Rhodes J, Abdolrasouli A, Farrer RA, Cuomo CA, Aanensen DM, Armstrong-James D, et al. Genomic epidemiology of the UK outbreak of the emerging human fungal pathogen Candida auris. Emerg Microbes Infect. 2018;7: 43. doi: 10.1038/s41426-018-0045-x 29593275
25. Muñoz JF, Gade L, Chow NA, Loparev VN, Juieng P, Berkow EL, et al. Genomic insights into multidrug-resistance, mating and virulence in Candida auris and related emerging species. Nat Commun. Nature Publishing Group; 2018;9: 5346. doi: 10.1038/s41467-018-07779-6 30559369
26. Sarma S, Upadhyay S. Current perspective on emergence, diagnosis and drug resistance in Candida auris. Infect Drug Resist. 2017;10: 155–165. doi: 10.2147/IDR.S116229 28652784
27. Henry KW, Nickels JT, Edlind TD. Upregulation of ERG genes in Candida species by azoles and other sterol biosynthesis inhibitors. Antimicrob Agents Chemother. 2000;44: 2693–2700. doi: 10.1128/aac.44.10.2693-2700.2000 10991846
28. Kolondra A, Labedzka-Dmoch K, Wenda JM, Drzewicka K, Golik P. The transcriptome of Candida albicans mitochondria and the evolution of organellar transcription units in yeasts. BMC Genomics. 2015;16: 827. doi: 10.1186/s12864-015-2078-z 26487099
29. Saris K, Meis JF, Voss A. Candida auris. Curr Opin Infect Dis. 2018;31: 334–340. doi: 10.1097/QCO.0000000000000469 29878905
30. Chowdhary A, Sharma C, Meis JF. Candida auris: A rapidly emerging cause of hospital-acquired multidrug-resistant fungal infections globally. Hogan DA, editor. PLoS Pathog. Public Library of Science; 2017;13: e1006290. doi: 10.1371/journal.ppat.1006290 28542486
31. Luo G, Ibrahim AS, Spellberg B, Nobile CJ, Mitchell AP, Fu Y. Candida albicans Hyr1p confers resistance to neutrophil killing and is a potential vaccine target. J Infect Dis. 2010;201: 1718–1728. doi: 10.1086/652407 20415594
32. Luo G, Ibrahim AS, French SW, Edwards JE, Fu Y. Active and passive immunization with rHyr1p-N protects mice against hematogenously disseminated candidiasis. PLoS ONE. 2011;6: e25909. doi: 10.1371/journal.pone.0025909 22028796
33. Dwivedi P, Thompson A, Xie Z, Kashleva H, Ganguly S, Mitchell AP, et al. Role of Bcr1-activated genes Hwp1 and Hyr1 in Candida albicans oral mucosal biofilms and neutrophil evasion. PLoS ONE. 2011;6: e16218. doi: 10.1371/journal.pone.0016218 21283544
34. Hoyer LL, Green CB, Oh S-H, Zhao X. Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family—a sticky pursuit. Med Mycol. 2008;46: 1–15. doi: 10.1080/13693780701435317
35. Hoyer LL. The ALS gene family of Candida albicans. Trends Microbiol. 2001;9: 176–180. doi: 10.1016/s0966-842x(01)01984-9 11286882
36. Murciano C, Moyes DL, Runglall M, Tobouti P, Islam A, Hoyer LL, et al. Evaluation of the role of Candida albicans agglutinin-like sequence (Als) proteins in human oral epithelial cell interactions. PLoS ONE. 2012;7: e33362. doi: 10.1371/journal.pone.0033362 22428031
37. Koskiniemi S, Sun S, Berg OG, Andersson DI. Selection-driven gene loss in bacteria. PLoS Genet. 2012;8: e1002787. doi: 10.1371/journal.pgen.1002787 22761588
38. Fitzpatrick DA. Horizontal gene transfer in fungi. FEMS Microbiol Lett. 2012;329: 1–8. doi: 10.1111/j.1574-6968.2011.02465.x 22112233
39. Oh BJ, Shin JH, Kim M-N, Sung H, Lee K, Joo MY, et al. Biofilm formation and genotyping of Candida haemulonii, Candida pseudohaemulonii, and a proposed new species (Candida auris) isolates from Korea. Med Mycol. 2011;49: 98–102. doi: 10.3109/13693786.2010.493563 20560864
40. Yang F, Kravets A, Bethlendy G, Welle S, Rustchenko E. Chromosome 5 monosomy of Candida albicans controls susceptibility to various toxic agents, including major antifungals. Antimicrob Agents Chemother. 2013;57: 5026–5036. doi: 10.1128/AAC.00516-13 23896475
41. Yang F, Zhang L, Wakabayashi H, Myers J, Jiang Y, Cao Y, et al. Tolerance to Caspofungin in Candida albicans Is Associated with at Least Three Distinctive Mechanisms That Govern Expression of FKS Genes and Cell Wall Remodeling. Antimicrob Agents Chemother. 2017;61. doi: 10.1128/AAC.00071-17 28223384
42. Ghannoum MA, Rice LB. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev. American Society for Microbiology (ASM); 1999;12: 501–517.
43. Perea S, Patterson TF. Antifungal resistance in pathogenic fungi. Clin Infect Dis. 2002;35: 1073–1080. doi: 10.1086/344058 12384841
44. Albertson GD, Niimi M, Cannon RD, Jenkinson HF. Multiple efflux mechanisms are involved in Candida albicans fluconazole resistance. Antimicrob Agents Chemother. American Society for Microbiology (ASM); 1996;40: 2835–2841.
45. Andersen JP, Vestergaard AL, Mikkelsen SA, Mogensen LS, Chalat M, Molday RS. P4-ATPases as Phospholipid Flippases-Structure, Function, and Enigmas. Front Physiol. Frontiers; 2016;7: 275. doi: 10.3389/fphys.2016.00275 27458383
46. Fisher MC, Hawkins NJ, Sanglard D, Gurr SJ. Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science. 2018;360: 739–742. doi: 10.1126/science.aap7999 29773744
47. Won EJ, Shin JH, Choi MJ, Lee WG, Park Y-J, Uh Y, et al. Antifungal susceptibilities of bloodstream isolates of Candida species from nine hospitals in Korea: application of new antifungal breakpoints and relationship to antifungal usage. Chaturvedi V, editor. PLoS ONE. 2015;10: e0118770. doi: 10.1371/journal.pone.0118770 25706866
48. Clinical and Laboratory Standards Institute. M27-A3: Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved standard 3rd ed. Wayne: Clinical and Laboratory Standard Institute.
49. Kato K, Hashino M, Ito T, Matsui M, Suzuki S, Kai K, et al. Rapid and affordable size-selected PacBio single-molecule real-time sequencing template library construction using the bead-beating DNA extraction method. Journal of Biological Methods. 2017;4: e79. doi: 10.14440/jbm.2017.169 31453233
50. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27: 722–736. doi: 10.1101/gr.215087.116 28298431
51. Li H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences. Bioinformatics. 2016;32: 2103–2110. doi: 10.1093/bioinformatics/btw152 27153593
52. Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 2017;27: 737–746. doi: 10.1101/gr.214270.116 28100585
53. Hunt M, Silva ND, Otto TD, Parkhill J, Keane JA, Harris SR. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol. 2015;16: 294. doi: 10.1186/s13059-015-0849-0 26714481
54. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE. 2014;9: e112963. doi: 10.1371/journal.pone.0112963 25409509
55. Aronesty E. Comparison of Sequencing Utility Programs. TOBIOIJ. 2013;7: 1–8. doi: 10.2174/1875036201307010001
56. Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics. 2015;31: 587–589. doi: 10.1093/bioinformatics/btu661 25338718
57. Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 2008;18: 1979–1990. doi: 10.1101/gr.081612.108 18757608
58. Laslett D, Canback B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 2004;32: 11–16. doi: 10.1093/nar/gkh152 14704338
59. Mistry J, Finn RD, Eddy SR, Bateman A, Punta M. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 2013;41: e121. doi: 10.1093/nar/gkt263 23598997
60. Haft DH, Selengut JD, Richter RA, Harkins D, Basu MK, Beck E. TIGRFAMs and Genome Properties in 2013. Nucleic Acids Res. 2013;41: D387–95. doi: 10.1093/nar/gks1234 23197656
61. Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 2002;30: 281–283. doi: 10.1093/nar/30.1.281 11752315
62. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45: D200–D203. doi: 10.1093/nar/gkw1129 27899674
63. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30: 1236–1240. doi: 10.1093/bioinformatics/btu031 24451626
64. Sharma C, Kumar N, Meis JF, Pandey R, Chowdhary A. Draft Genome Sequence of a Fluconazole-Resistant Candida auris Strain from a Candidemia Patient in India. Genome Announc. American Society for Microbiology; 2015;3: 41. doi: 10.1128/genomeA.00722-15 26184929
65. Chatterjee S, Alampalli SV, Nageshan RK, Chettiar ST, Joshi S, Tatu US. Draft genome of a commonly misdiagnosed multidrug resistant pathogen Candida auris. BMC Genomics. 2015;16: 686. doi: 10.1186/s12864-015-1863-z 26346253
66. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26: 589–595. doi: 10.1093/bioinformatics/btp698 20080505
67. Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, Mardis ER, et al. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics. 2009;25: 2283–2285. doi: 10.1093/bioinformatics/btp373 19542151
68. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5: R12. doi: 10.1186/gb-2004-5-2-r12 14759262
69. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22: 2688–2690. doi: 10.1093/bioinformatics/btl446 16928733
70. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44: W242–5. doi: 10.1093/nar/gkw290 27095192
71. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinformatics. 2013;14: 178–192. doi: 10.1093/bib/bbs017 22517427
72. Huson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S, et al. MEGAN Community Edition—Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data. PLoS Comput Biol. 2016;12: e1004957. doi: 10.1371/journal.pcbi.1004957
73. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26: 2460–2461. doi: 10.1093/bioinformatics/btq461 20709691
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