Phylogenetic relationship of Fusarium species isolated from keratitis using TEF1 and RPB2 gene sequences
-
Zeynab Yassin
,
Zahra Salehi
,
Mohammad Soleimani
,
Ensieh Lotfali
,
Mahsa Fattahi
,
Somayeh Sharifynia
Abstract
Background and Objectives: Fusarium species are known to be one of the common causes of keratitis. This study was conducted to identify Fusarium spp. causing keratitis and to investigate their genetic diversity using TEF1 and RPB2 gene sequences.
Materials and Methods: Twenty-four clinical isolates of Fusarium were isolated from the patient with keratitis. Phylogenetic analysis of two-locus of the 24 clinical isolates and three reference strains was carried out using the maximum parsimony and RAxML methods.
Results: Based on gene sequences of the 24 clinical isolates, 17, 4, and 3 isolates were identified as Fusarium solani species complex (FSSC), Fusarium fujikuroi species complex (FFSC), and Fusarium oxysporum, respectively. FFSC include F. proliferatum (n=1), F. globosum (n=1), F. verticillioides (n=1), and F. brevicatenulatum (n=1), respectively.
Conclusion: Given that sequence of a sole gene can be challenging and on the other hand, due to the high resistance to antifungal drugs, identification of Fusarium species is of substantial significance. In this study, by designing a novel set of primers for the RPB2 area and using TEF1 primer, we were able to differentiate 24 Fusarium spp. isolated from patients with keratitis.
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2. Spierer O, Dugar J, Miller D, O'Brien TP. Comparative antifungal susceptibility analysis of Candida albicans versus non-albicans Candida corneal isolates. Cornea 2015; 34: 576-579.
3. Tighnavard Bejarbane R, Daie Ghazvini R, Mahmoudi S, Soltani Moghaddam R, Safara M, Bakhshi H, et al. Diagnosis of fungal keratitis in patients with corneal lesions at Amiralmomenin hospital in Rasht, Iran. TUMSJ 2017; 75: 374-380.
4. Garg P, Roy A, Roy S. Update on fungal keratitis. Curr Opin Ophthalmol 2016; 27: 333-339.
5. Haghani I, Amirinia F, Nowroozpoor-Dailami K, Shokohi T. Detection of fungi by conventional methods and semi-nested PCR in patients with presumed fungal keratitis. Curr Med Mycol 2015; 1: 31-38.
6. Badali H, Cañete-Gibas C, Patterson H, Sanders C, Mermella B, Garcia V, et all. In vitro activity of olorofim against clinical isolates of the Fusarium oxysporum and Fusarium solani species complexes. Mycoses 2021; 64: 748-752.
7. Ahmadikia K, Aghaei Gharehbolagh S, Fallah B, Naeimi Eshkaleti M, Malekifar P, Rahsepar S, et al. Distribution, prevalence, and causative agents of fungal keratitis: a systematic review and meta-analysis (1990 to 2020). Front Cell Infect Microbiol 2021; 11: 698780.
8. Dallé da Rosa P, Nunes A, Borges R, Batista B, Fuentefria AM, Goldani LZ. In vitro susceptibility and multilocus sequence typing of Fusarium isolates causing keratitis. J Mycol Med 2018; 28: 482-485.
9. Badali H, Patterson HP, Sanders CJ, Mermella B, Gibas CFC, Ibrahim AS, et all. Manogepix, the active moiety of the investigational agent Fosmanogepix, demonstrates in vitro activity against members of the Fusarium oxysporum and Fusarium solani species complexes. Antimicrob Agents Chemother 2021; 65:(6) e02343-20.
10. O'Donnell K, Sutton DA, Rinaldi MG, Gueidan C, Crous PW, Geiser DM. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. J Clin Microbiol 2009; 47: 3851-3861.
11. Oechsler RA, Yamanaka TM, Bispo PJ, Sartori J, Yu MC, Melo AS, et al. Fusarium keratitis in Brazil: genotyping, in vitro susceptibilities, and clinical outcomes. Clin Ophthalmol 2013; 7: 1693-1701.
12. O'Donnell K, Sutton DA, Rinaldi MG, Magnon KC, Cox PA, Revankar SG, et al. Genetic diversity of human pathogenic members of the Fusarium oxysporum complex inferred from multilocus DNA sequence data and amplified fragment length polymorphism analyses: evidence for the recent dispersion of a geographically widespread clonal lineage and nosocomial origin. J Clin Microbiol 2004; 42: 5109-5120.
13. Sandoval-Denis M, Lombard L, Crous PW. Back to the roots: a reappraisal of Neocosmospora. Persoonia 2019; 43: 90-185.
14. Summerbell RC, Schroers HJ. Analysis of phylogenetic relationship of Cylindrocarpon lichenicola and Acremonium falciforme to the Fusarium solani species complex and a review of similarities in the spectrum of opportunistic infections caused by these fungi. J Clin Microbiol 2002; 40: 2866-2875.
15. Zhang N, O'Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, et al. Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol 2006; 44: 2186-2190.
16. Schroers HJ, Samuels GJ, Zhang N, Short DP, Juba J, Geiser DM. Epitypification of Fusisporium (Fusarium) solani and its assignment to a common phylogenetic species in the Fusarium solani species complex. Mycologia 2016; 108: 806-819.
17. Al-Hatmi AM, van Diepeningen AD, Curfs-Breuker I, de Hoog GS, Meis JF. Specific antifungal susceptibility profiles of opportunists in the Fusarium fujikuroi complex. J Antimicrob Chemother 2015; 70: 1068-1071.
18. O'Donnell K, Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME, et al. Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 2008; 46: 2477-2490.
19. Schroers HJ, O’Donnell K, Lamprecht SC, Kammeyer PL, Johnson S, Sutton DA, et al. Taxonomy and phylogeny of the Fusarium dimerum species group. Mycologia 2009; 101: 44-70.
20. O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, et al. A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet Biol 2009; 46: 936-948.
21. O’Donnell K, Ward TJ, Robert VA, Crous PW, Geiser DM, Kang S. DNA sequence-based identification of Fusarium: current status and future directions. Phytoparasitica 2015; 43: 583-595.
22. Thomas PA, Kaliamurthy J. Mycotic keratitis: epidemiology, diagnosis and management. Clin Microbiol Infect 2013; 19: 210-220.
23. Salehi Z, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Antifungal drug susceptibility profile of clinically important dermatophytes and determination of point mutations in terbinafine-resistant isolates. Eur J Clin Microbiol Infect Dis 2018; 37: 1841-1846.
24. Senatore MT, Ward TJ, Cappelletti E, Beccari G, McCormick SP, Busman M, et al. Species diversity and mycotoxin production by members of the Fusarium tricinctum species complex associated with Fusarium head blight of wheat and barley in Italy. Int J Food Microbiol 2021; 358: 109298.
25. Kumar S, Tamura K, Jakobsen IB, Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 2001; 17: 1244-1245.
26. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312-1313.
27. Hunter PR. Reproducibility and indices of discriminatory power of microbial typing methods. J Clin Microbiol 1990; 28: 1903-1905.
28. Sun S, Lui Q, Han L, Ma Q, He S, Li X, et al. Identification and characterization of Fusarium proliferatum, a new species of fungi that cause fungal keratitis. Sci Rep 2018; 8: 4859.
29. O'Donnell K, Sutton DA, Rinaldi MG, Sarver BAJ, Balajee SA, Schroers HJ, et al. Internet-accessible dna sequence database for identifying Fusaria from human and animal infections. J Clin Microbiol 2010; 48: 3708-3718.
2. Spierer O, Dugar J, Miller D, O'Brien TP. Comparative antifungal susceptibility analysis of Candida albicans versus non-albicans Candida corneal isolates. Cornea 2015; 34: 576-579.
3. Tighnavard Bejarbane R, Daie Ghazvini R, Mahmoudi S, Soltani Moghaddam R, Safara M, Bakhshi H, et al. Diagnosis of fungal keratitis in patients with corneal lesions at Amiralmomenin hospital in Rasht, Iran. TUMSJ 2017; 75: 374-380.
4. Garg P, Roy A, Roy S. Update on fungal keratitis. Curr Opin Ophthalmol 2016; 27: 333-339.
5. Haghani I, Amirinia F, Nowroozpoor-Dailami K, Shokohi T. Detection of fungi by conventional methods and semi-nested PCR in patients with presumed fungal keratitis. Curr Med Mycol 2015; 1: 31-38.
6. Badali H, Cañete-Gibas C, Patterson H, Sanders C, Mermella B, Garcia V, et all. In vitro activity of olorofim against clinical isolates of the Fusarium oxysporum and Fusarium solani species complexes. Mycoses 2021; 64: 748-752.
7. Ahmadikia K, Aghaei Gharehbolagh S, Fallah B, Naeimi Eshkaleti M, Malekifar P, Rahsepar S, et al. Distribution, prevalence, and causative agents of fungal keratitis: a systematic review and meta-analysis (1990 to 2020). Front Cell Infect Microbiol 2021; 11: 698780.
8. Dallé da Rosa P, Nunes A, Borges R, Batista B, Fuentefria AM, Goldani LZ. In vitro susceptibility and multilocus sequence typing of Fusarium isolates causing keratitis. J Mycol Med 2018; 28: 482-485.
9. Badali H, Patterson HP, Sanders CJ, Mermella B, Gibas CFC, Ibrahim AS, et all. Manogepix, the active moiety of the investigational agent Fosmanogepix, demonstrates in vitro activity against members of the Fusarium oxysporum and Fusarium solani species complexes. Antimicrob Agents Chemother 2021; 65:(6) e02343-20.
10. O'Donnell K, Sutton DA, Rinaldi MG, Gueidan C, Crous PW, Geiser DM. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. J Clin Microbiol 2009; 47: 3851-3861.
11. Oechsler RA, Yamanaka TM, Bispo PJ, Sartori J, Yu MC, Melo AS, et al. Fusarium keratitis in Brazil: genotyping, in vitro susceptibilities, and clinical outcomes. Clin Ophthalmol 2013; 7: 1693-1701.
12. O'Donnell K, Sutton DA, Rinaldi MG, Magnon KC, Cox PA, Revankar SG, et al. Genetic diversity of human pathogenic members of the Fusarium oxysporum complex inferred from multilocus DNA sequence data and amplified fragment length polymorphism analyses: evidence for the recent dispersion of a geographically widespread clonal lineage and nosocomial origin. J Clin Microbiol 2004; 42: 5109-5120.
13. Sandoval-Denis M, Lombard L, Crous PW. Back to the roots: a reappraisal of Neocosmospora. Persoonia 2019; 43: 90-185.
14. Summerbell RC, Schroers HJ. Analysis of phylogenetic relationship of Cylindrocarpon lichenicola and Acremonium falciforme to the Fusarium solani species complex and a review of similarities in the spectrum of opportunistic infections caused by these fungi. J Clin Microbiol 2002; 40: 2866-2875.
15. Zhang N, O'Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, et al. Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol 2006; 44: 2186-2190.
16. Schroers HJ, Samuels GJ, Zhang N, Short DP, Juba J, Geiser DM. Epitypification of Fusisporium (Fusarium) solani and its assignment to a common phylogenetic species in the Fusarium solani species complex. Mycologia 2016; 108: 806-819.
17. Al-Hatmi AM, van Diepeningen AD, Curfs-Breuker I, de Hoog GS, Meis JF. Specific antifungal susceptibility profiles of opportunists in the Fusarium fujikuroi complex. J Antimicrob Chemother 2015; 70: 1068-1071.
18. O'Donnell K, Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME, et al. Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 2008; 46: 2477-2490.
19. Schroers HJ, O’Donnell K, Lamprecht SC, Kammeyer PL, Johnson S, Sutton DA, et al. Taxonomy and phylogeny of the Fusarium dimerum species group. Mycologia 2009; 101: 44-70.
20. O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, et al. A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet Biol 2009; 46: 936-948.
21. O’Donnell K, Ward TJ, Robert VA, Crous PW, Geiser DM, Kang S. DNA sequence-based identification of Fusarium: current status and future directions. Phytoparasitica 2015; 43: 583-595.
22. Thomas PA, Kaliamurthy J. Mycotic keratitis: epidemiology, diagnosis and management. Clin Microbiol Infect 2013; 19: 210-220.
23. Salehi Z, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Antifungal drug susceptibility profile of clinically important dermatophytes and determination of point mutations in terbinafine-resistant isolates. Eur J Clin Microbiol Infect Dis 2018; 37: 1841-1846.
24. Senatore MT, Ward TJ, Cappelletti E, Beccari G, McCormick SP, Busman M, et al. Species diversity and mycotoxin production by members of the Fusarium tricinctum species complex associated with Fusarium head blight of wheat and barley in Italy. Int J Food Microbiol 2021; 358: 109298.
25. Kumar S, Tamura K, Jakobsen IB, Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 2001; 17: 1244-1245.
26. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312-1313.
27. Hunter PR. Reproducibility and indices of discriminatory power of microbial typing methods. J Clin Microbiol 1990; 28: 1903-1905.
28. Sun S, Lui Q, Han L, Ma Q, He S, Li X, et al. Identification and characterization of Fusarium proliferatum, a new species of fungi that cause fungal keratitis. Sci Rep 2018; 8: 4859.
29. O'Donnell K, Sutton DA, Rinaldi MG, Sarver BAJ, Balajee SA, Schroers HJ, et al. Internet-accessible dna sequence database for identifying Fusaria from human and animal infections. J Clin Microbiol 2010; 48: 3708-3718.
| Files | ||
| Issue | Vol 14 No 3 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i3.9794 | |
| Keywords | ||
| Keratitis; Fusarium oxysporum; Fusarium solani species complex; Fusarium fujikuroi species complex | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Yassin Z, Salehi Z, Soleimani M, Lotfali E, Fattahi M, Sharifynia S. Phylogenetic relationship of Fusarium species isolated from keratitis using TEF1 and RPB2 gene sequences. Iran J Microbiol. 2022;14(3):417-422.
