Comparative genomics of opportunistic Phialophora species involved in divergent disease types.
CARD Signaling Adaptor Proteins
/ immunology
Candidiasis
/ microbiology
Chromoblastomycosis
/ immunology
Fungal Proteins
/ genetics
Genome, Fungal
Genomics
Humans
Immunocompromised Host
/ immunology
Opportunistic Infections
/ immunology
Phaeohyphomycosis
/ immunology
Phialophora
/ genetics
Phylogeny
CARD9 gene mutation
Chromoblastomycosis
PKS domains
Phialophora verrucosa complex
comparative genomics
phaeohyphomycosis
Journal
Mycoses
ISSN: 1439-0507
Titre abrégé: Mycoses
Pays: Germany
ID NLM: 8805008
Informations de publication
Date de publication:
May 2021
May 2021
Historique:
revised:
10
01
2021
received:
26
12
2020
accepted:
11
01
2021
pubmed:
18
1
2021
medline:
22
9
2021
entrez:
17
1
2021
Statut:
ppublish
Résumé
Black opportunists Phialophora verrucosa complex species can cause different disease types in competent and in immunocompromised individuals, but are remarkably overrepresented in CARD9-related infections. To better understand the ecology and potential pathogenicity of opportunistic Phialophora species and reveal eventual genetic parameters associated with the behaviour in vivo and genetic profiles in patients with CARD9 immunodeficiency. Genomes of 26 strains belonging to six species of the Phialophora verrucosa complex were sequenced. Using multilocus analysis, all environmental and clinical strains were identified correctly. We compared the genomes of agents from different disease types among each other including CARD9 immunodeficiency. We obtained genome sizes of the 26 Phialophora strains ranged between 32 and 37 MB. Some species showed considerable intraspecific genomic variation. P americana showed the highest degree of variability. P verrucosa was variable in CAZy enzymes, whereas P americana varied in PKS-related genes. Phialophora species, particularly P verrucosa, are relatively frequent in patients with CARD9-related immunodeficiency. Different mutations in the CARD9 gene seem to increase susceptibility for infection by different groups of species, that is either Candida, dermatophytes or black fungi. A number of patients with chromoblastomycosis revealed an as yet unknown CARD9 mutation. TNFα impairment was prevalent in patients with CARD9 infections, while CBM patients were invariably IFNγ. From genomic investigations, the known virulence factors between clinical and environmental strains did not reveal any significant difference. Phialophora complex has an equal chance to cause infection in humans, either healthy or CARD9-impaired.
Sections du résumé
BACKGROUND
BACKGROUND
Black opportunists Phialophora verrucosa complex species can cause different disease types in competent and in immunocompromised individuals, but are remarkably overrepresented in CARD9-related infections.
OBJECTIVES
OBJECTIVE
To better understand the ecology and potential pathogenicity of opportunistic Phialophora species and reveal eventual genetic parameters associated with the behaviour in vivo and genetic profiles in patients with CARD9 immunodeficiency.
METHODS
METHODS
Genomes of 26 strains belonging to six species of the Phialophora verrucosa complex were sequenced. Using multilocus analysis, all environmental and clinical strains were identified correctly. We compared the genomes of agents from different disease types among each other including CARD9 immunodeficiency.
RESULTS
RESULTS
We obtained genome sizes of the 26 Phialophora strains ranged between 32 and 37 MB. Some species showed considerable intraspecific genomic variation. P americana showed the highest degree of variability. P verrucosa was variable in CAZy enzymes, whereas P americana varied in PKS-related genes. Phialophora species, particularly P verrucosa, are relatively frequent in patients with CARD9-related immunodeficiency. Different mutations in the CARD9 gene seem to increase susceptibility for infection by different groups of species, that is either Candida, dermatophytes or black fungi. A number of patients with chromoblastomycosis revealed an as yet unknown CARD9 mutation. TNFα impairment was prevalent in patients with CARD9 infections, while CBM patients were invariably IFNγ.
CONCLUSIONS
CONCLUSIONS
From genomic investigations, the known virulence factors between clinical and environmental strains did not reveal any significant difference. Phialophora complex has an equal chance to cause infection in humans, either healthy or CARD9-impaired.
Substances chimiques
CARD Signaling Adaptor Proteins
0
Fungal Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
555-568Subventions
Organisme : National Natural Science Foundation of China
ID : 31670145
Organisme : National Natural Science Foundation of China
ID : 81902043
Organisme : International Cooperation and Exchanges Project
ID : 81520108026
Informations de copyright
© 2021 Wiley-VCH GmbH.
Références
De Hoog GS, Guarro J, Gené J, et al. Atlas of clinical fungi, 4th edn. Hilversum, The Netherlands: Foundation Atlas of Clinical Fungi; 2020.
Queiroz-Telles F, de Hoog S, Santos DW, et al. Chromoblastomycosis. Clin Rev Microbiol. 2017;30:233-276.
Vaezi A, Fakhim H, Abtahian Z, et al. Frequency and geographic distribution of CARD9 mutations in patients with severe fungal infections. Front Microbiol. 2018;9:2434.
Song Y, Du M, da Menezes Silva N, et al. Comparative analysis of the black yeast Exophiala spinifera from a CARD9 deficiency patient combining short- and long-read genome sequencing technology. Front Microbiol. 2020;11:1880.
Ahmed SA, Bonifaz A, González GM, et al. Chromoblastomycosis caused by Phialophora - proven cases from Mexico. J Fungi. 2021, Submitted.
Kimura M, Goto A, Furuta T, Satou T, Hashimoto S, Nishimura K. Multifocal subcutaneous phaeohyphomycosis caused by Phialophora verrucosa. Arch Path Lab Med. 2003;127:91-93.
Ohira S, Isoda K, Hamanaka H, Takahashi K, Nishimoto K, Mizutani H. Phaeohyphomycosis caused by Phialophora verrucosa developed in a patient with non-HIV acquired immunodeficiency syndrome. Mycoses. 2002;45:50-54.
Li Y, Xiao J, de Hoog GS, et al. Biodiversity and human-pathogenicity of Phialophora verrucosa and relatives in Chaetothyriales. Persoonia. 2016;38:1-19.
Huang C, Shan W, An K, et al. First report of chromoblastomycosis caused by Phialophora expanda in a Chinese CARD9-deficient patient. Chin J Mycol. 2020;15:230-232.
Huang C, Zhang Y, Song Y, Wan Z, Wang X, Li R. Phaeohyphomycosis caused by Phialophora americana with CARD9 mutation and 20-year literature review in China. Mycoses. 2019;62:908-919.
Hofmann H, Choi SM, Wilsmann-Theis D, Horré R, Bieber T, de Hoog GS Phialophora verrucosa causing invasive chromoblastomycosis and sinusitis in a child from northern Africa. Mycoses. 2005;48:456-461.
Chin CS, Alexander DH, Marks P, et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods. 2013;10:563-569.
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.
Lam KK, LaButti K, Khalak A, Tse D. FinisherSC: a repeat-aware tool for upgrading de novo assembly using long reads. Bioinformatics (Oxford). 2015;31:3207-3209.
Bankevich A, Nurk S, Antipov D, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455-477.
Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. In: Kollmar M (eds), Gene Prediction. Methods Molec Biol 1962. New York, NY: Humana; 2019.
Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, Borodovsky M. Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 2005;33:6494-6506.
Quevillon E, Silventoinen V, Pillai S, et al. InterProScan: protein domains identifier. Nucleic Acids Res. 2005;33:W116-W120.
Zhang H, Yohe T, Huang L, et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95-W101.
Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16:157.
Quan Y, Muggia L, Moreno LF, et al. A re-evaluation of the Chaetothyriales using criteria of phylogeny and ecology. Fung Div. 2020;103:47-85.
Kumar S, Stecher G, Peterson D, Tamura K. MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics. 2012;28:2685-2686.
Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 1999;Ser 41:95-98.
Wiens JJ. Missing data and the design of phylogenetic analyses. J Biomed Inform. 2006;39:34-42.
Wiens JJ. Missing data and the accuracy of Bayesian phylogenetics. J Syst Evol. 2008;46:307-314.
Criscuolo A. A fast alignment-free bioinformatics procedure to infer accurate distance-based phylogenetic trees from genome assemblies. Res Ideas Outcomes. 2019;5:e36178.
Zhang R, Wang X, Wan Z, Li R. CARD9 mutations and related immunological research of one case with disseminated phaeohyphomycosis. J Microbes Infect. 2017;12:14-23.
Wang X, Wang W, Lin Z, et al. CARD9 mutations linked to subcutaneous phaeohyphomycosis and TH17 cell deficiencies. J Allergy Clin Immunol. 2014;133(3):905-908.e3.
Lanternier F, Barbati E, Meinzer U, et al. Inherited CARD9 deficiency in 2 unrelated patients with invasive Exophiala infection. J Infect Dis. 2015;211:1241-1250.
Wang X, Zhang R, Wu W, et al. Impaired specific antifungal immunity in CARD9-deficient patients with phaeohyphomycosis. J Invest Dermatol. 2017;138:3.
Sobianski Herman T, Gomes RR, Queiroz Telles F, Pedroso CA, Vicente VA. Identification of CARD9 mutation in patients with chromoblastomycosis and evaluation of the immunological response. 2021 (submitted).
Yan XX, Yu CP, Fu XA, et al. CARD9 mutation linked to Corynespora cassiicola infection in a Chinese patient. Br J Dermatol. 2016;174:176-179.
Arango-Franco CA, Moncada-Vélez M, Beltrán CP, et al. Early-onset invasive infection due to Corynespora cassiicola associated with compound heterozygous CARD9 mutations in a Colombian patient. J Clin Immunol. 2018;38:794-803.
Medlar EM. A new fungus, Phialophora verrucosa, pathogenic for man. Mycologia. 1915;7:200-203.
Attili-Angelis D, Duarte APM, Pagnocca FC, et al. Novel Phialophora species from leaf-cutting ants (tribe Attini). Fung Div. 2014;65:65-75.
Song Y, Menezes da Silva N, Vu D, et al. Comparative genomic analysis of capsule-producing black yeasts Exophiala dermatitidis and E spinifera, potential agents of disseminated mycoses. Front Microbiol. 2020;11:586.
Zhou X, Huang M, Ma Z. Comparative genomic data provide new insight on the evolution of pathogenicity in Sporothrix species. Front Microbiol. 2020;11:e565439.
Zheng H, Blechert O, Mei H, et al. Whole-genome resequencing of Trichophyton rubrum provides insights into population differentiation and drug resistance. Mycopathologia. 2020;185:103-112.
Li DM, Li RY, de Hoog GS, Sudhadham M, Wang DL. Fatal Exophiala infections in China, with a report of seven cases. Mycoses. 2011;54:136-142.
Matos T, de Hoog GS, de Boer AG, de Crom I, Haase G. High prevalence of the neurotrope Exophiala dermatitidis and related oligotrophic black yeasts in sauna facilities. Mycoses. 2002;45:373-377.
Drummond RA, Lionakis MS. Mechanistic insights into the role of C-type lectin receptor / CARD9 signaling in human antifungal immunity. Front Cell Infect Microbiol. 2016;6:39.
Chang X, Li R, Yu J, Bao X, Qin J. Phaeohyphomycosis of the central nervous system caused by Exophiala dermatitidis in a 3-year-old immunocompetent host. J Child Neurol. 2009;24:342-345.
Mitchell DM, Fitz-Henley M, Horner-Bryce J. A case of disseminated phaeohyphomycosis caused by Cladosporium devriesii. West Ind Med J. 1990;39:118-123.
Bonifaz A, Davoudi MM, de Hoog GS, et al. Severe disseminated phaeohyphomycosis in an immunocompetent patient caused by Veronaea botryosa. Mycopathologia. 2013;175:497-503.
Santos DW, Camargo LF, Gonçalves SS, et al. Melanized fungal infections in kidney transplant recipients: contributions to optimize clinical management. Clin Microbiol Infect. 2017;23:333, e9-333.e14.17.
Drewniak A, Gazendam RP, Tool ATJ, et al. Invasive fungal infection and impaired neutrophil killing in human CARD9 deficiency. Blood. 2013;28(121):2385-2392.
De Bruyne M, Hoste L, Bogaert DJ, et al. A CARD9 founder mutation disrupts NF-kappaB signaling by inhibiting BCL10 and MALT1 recruitment and signalosome formation. Front Immunol. 2018;9:2366.
Rosentul DC, Plantinga TS, Oosting M, et al. Genetic variation in the dectin-1/CARD9 recognition pathway and susceptibility to candidemia. J Infect Dis. 2011;204:1138-1145.
Surash S, Tyagi A, de Hoog GS, Zeng JS, Barton RC, Hobson RP. Cerebral phaeohyphomycosis caused by Fonsecaea monophora. Med Mycol. 2005;43:465-472.
Perez L, Messina F, Negroni R, et al. Inherited CARD9 deficiency in a patient with both Exophiala spinifera and Aspergillus nomius severe infections. J Clin Immunol. 2020;40:359-366.
Wang C, Xing H, Jiang X, et al. Cerebral phaeohyphomycosis caused by Exophiala dermatitidis in a Chinese CARD9-deficient patient: a case report and literature review. Front Neurol. 2019;10:938.