The Emergence of New Sporothrix brasiliensis Genotypes in Current Epidemic of Sporotrichosis in Southeastern Brazil.
AFLP
genetic diversity
mating type
molecular epidemiology
sporotrichosis
Journal
Mycoses
ISSN: 1439-0507
Titre abrégé: Mycoses
Pays: Germany
ID NLM: 8805008
Informations de publication
Date de publication:
Sep 2024
Sep 2024
Historique:
revised:
21
08
2024
received:
09
06
2024
accepted:
22
08
2024
medline:
9
9
2024
pubmed:
9
9
2024
entrez:
9
9
2024
Statut:
ppublish
Résumé
Zoonotic sporotrichosis caused by Sporothrix brasiliensis has become the main subcutaneous mycosis in Brazil. Minas Gerais (MG) is located in southeast Brazil and since 2015 has experienced an epidemic of zoonotic sporotrichosis. This study aimed to reconstruct the epidemiological scenario of sporotrichosis from S. brasiliensis in recent epizooty in the Metropolitan Region of Belo Horizonte (MRBH), MG. A total of 95 Sporothrix spp. isolates (Sporothirx brasiliensis n = 74, S. schenckii n = 11 and S. globosa n = 10) were subjected to Amplified Fragment Length Polymorphism (AFLP) genotyping and mating-type analysis to determine genetic diversity and population structure. Of these, 46 S. brasiliensis isolates were recovered from animals (cats n = 41 and dogs n = 5) from MRBH. Our study describes the high interspecific differentiation power of AFLP-based genotyping between the main phylogenetic Sporothrix groups. S. brasiliensis presents high genetic variability and pronounced population structure with geographically focused outbreaks in Brazil. The genetic groups include older genotypes from the prolonged epidemic in Southeast (Rio de Janeiro and São Paulo), South (Rio Grande do Sul), Northeast (Pernambuco) and new genotypes from the MRBH. Furthermore, we provide evidence of heterothallism mating strategy in pathogenic Sporothrix species. Genotypes originating in Rio de Janeiro and Pernambuco carry the predominant MAT1-2 idiomorph as opposed to genotypes from Rio Grande do Sul, which have the MAT1-1 idiomorph. We observed an overwhelming occurrence of MAT1-1 among MRBH isolates. Our study provides clear evidence of the predominance of a genetic group profile circulating in animals in Minas Gerais, independent of that disseminated from Rio de Janeiro. Our data can help us understand the genetic population processes that drive the evolution of this fungus in Minas Gerais and contribute to future mitigation actions for this ongoing epidemic.
Sections du résumé
BACKGROUND
BACKGROUND
Zoonotic sporotrichosis caused by Sporothrix brasiliensis has become the main subcutaneous mycosis in Brazil. Minas Gerais (MG) is located in southeast Brazil and since 2015 has experienced an epidemic of zoonotic sporotrichosis.
OBJECTIVES
OBJECTIVE
This study aimed to reconstruct the epidemiological scenario of sporotrichosis from S. brasiliensis in recent epizooty in the Metropolitan Region of Belo Horizonte (MRBH), MG.
METHODS
METHODS
A total of 95 Sporothrix spp. isolates (Sporothirx brasiliensis n = 74, S. schenckii n = 11 and S. globosa n = 10) were subjected to Amplified Fragment Length Polymorphism (AFLP) genotyping and mating-type analysis to determine genetic diversity and population structure. Of these, 46 S. brasiliensis isolates were recovered from animals (cats n = 41 and dogs n = 5) from MRBH.
RESULTS
RESULTS
Our study describes the high interspecific differentiation power of AFLP-based genotyping between the main phylogenetic Sporothrix groups. S. brasiliensis presents high genetic variability and pronounced population structure with geographically focused outbreaks in Brazil. The genetic groups include older genotypes from the prolonged epidemic in Southeast (Rio de Janeiro and São Paulo), South (Rio Grande do Sul), Northeast (Pernambuco) and new genotypes from the MRBH. Furthermore, we provide evidence of heterothallism mating strategy in pathogenic Sporothrix species. Genotypes originating in Rio de Janeiro and Pernambuco carry the predominant MAT1-2 idiomorph as opposed to genotypes from Rio Grande do Sul, which have the MAT1-1 idiomorph. We observed an overwhelming occurrence of MAT1-1 among MRBH isolates.
CONCLUSION
CONCLUSIONS
Our study provides clear evidence of the predominance of a genetic group profile circulating in animals in Minas Gerais, independent of that disseminated from Rio de Janeiro. Our data can help us understand the genetic population processes that drive the evolution of this fungus in Minas Gerais and contribute to future mitigation actions for this ongoing epidemic.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13792Subventions
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
Organisme : The Nacional Institute of Science and Technology in Human Pathogenic Fungi, Brazil
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
Organisme : Fundação de Amparo à Pesquisa do Estado de Minas Gerais
Informations de copyright
© 2024 Wiley‐VCH GmbH. Published by John Wiley & Sons Ltd.
Références
R. Almeida‐Paes, M. M. E. de Oliveira, D. F. S. Freitas, A. C. F. do Valle, R. M. Zancopé‐Oliveira, and M. C. Gutierrez‐Galhardo, “Sporotrichosis in Rio de Janeiro, Brazil: Sporothrix brasiliensis is Associated With Atypical Clinical Presentations,” PLoS Neglected Tropical Diseases 8 (2014): e3094, https://doi.org/10.1371/journal.pntd.0003094.
V. C. R. Magalhães, S. A. Colombo, N. T. A. Peres, et al., “Clinical Factors Associated With Systemic Sporotrichosis in Brazil,” Mycoses 67 (2024): e13656, https://doi.org/10.1111/myc.13656.
I. D. F. Gremião, M. M. E. Oliveira, L. H. Monteiro de Miranda, D. F. Saraiva Freitas, and S. A. Pereira, “Geographic Expansion of Sporotrichosis, Brazil,” Emerging Infectious Diseases 26 (2020): 621–624, https://doi.org/10.3201/eid2603.190803.
A. M. Rodrigues, S. S. Gonçalves, J. A. de Carvalho, L. P. Borba‐Santos, S. Rozental, and Z. P. Camargo, “Current Progress on Epidemiology, Diagnosis, and Treatment of Sporotrichosis and Their Future Trends,” Journal of Fungi 8 (2022): 776, https://doi.org/10.3390/jof8080776.
T. M. Brandolt, I. M. Madrid, V. R. Poester, et al., “Human Sporotrichosis: A Zoonotic Outbreak in Southern Brazil, 2012–2017,” Medical Mycology 57 (2019): 527–533, https://doi.org/10.1093/mmy/myy082.
V. R. Poester, R. P. Basso, D. A. Stevens, et al., “Treatment of Human Sporotrichosis Caused by Sporothrix brasiliensis,” Journal of Fungi 8 (2022): 70, https://doi.org/10.3390/jof8010070.
R. Orofino‐Costa, P. M. Macedo, A. M. Rodrigues, and A. R. Bernardes‐Engemann, “Sporotrichosis: An Update on Epidemiology, Etiopathogenesis, Laboratory and Clinical Therapeutics,” Anais Brasileiros de Dermatologia 92 (2017): 606–620, https://doi.org/10.1590/abd1806‐4841.2017279.
J. A. de Carvalho, M. A. Beale, F. Hagen, et al., “Trends in the Molecular Epidemiology and Population Genetics of Emerging Sporothrix Species,” Studies in Mycology 100 (2021): 100129, https://doi.org/10.1016/j.simyco.2021.100129.
A. M. Rodrigues, T. M. de Melo, G. S. de Hoog, et al., “Phylogenetic Analysis Reveals a High Prevalence of Sporothrix brasiliensis in Feline Sporotrichosis Outbreaks,” PLoS Neglected Tropical Diseases 7, no. 6 (2013): e2281, https://doi.org/10.1371/journal.pntd.0002281.
S. A. Colombo, G. C. Bicalho, C. S. F. de Oliveira, et al., “Emergence of Zoonotic Sporotrichosis due to Sporothrix brasiliensis in Minas Gerais, Brazil: A Molecular Approach to the Current Animal Disease,” Mycoses 66 (2023): 911–922, https://doi.org/10.1111/myc.13631.
A. Spanamberg, R. Araujo, A. P. Ravazzolo, D. Driemeier, R. M. S. Driemeier, and L. Ferreiro, “Sporothrix brasiliensis on Cats With Skin Ulcers in Southern Brazil,” Medical Mycology 59, no. 3 (2021): 301–304, https://doi.org/10.1093/mmy/myaa083.
H. Montenegro, A. M. Rodrigues, M. A. G. Dias, E. A. da Silva, F. Bernardi, and Z. P. de Camargo, “Feline Sporotrichosis Due to Sporothrix brasiliensis: An Emerging Animal Infection in São Paulo, Brazil,” BioMed Central Veterinary Research 10 (2014): 269, https://doi.org/10.1186/s12917‐014‐0269‐5.
A. Schubach, T. M. P. Schubach, M. B. Barros, et al., “Cat‐Transmitted Sporotrichosis, Rio de Janeiro, Brazil,” Emerging Infectious Diseases 11 (2005): 1952–1954, https://doi.org/10.3201/eid1112.040891.
B. A. de Oliveira, A. S. de Sena Costa, S. L. Lima, et al., “The Spread of cat‐Transmitted Sporotrichosis Due to Sporothrix brasiliensis in Brazil Towards the Northeast Region,” PLoS Neglected Tropical Diseases 15, no. 8 (2021): e0009693, https://doi.org/10.1371/journal.pntd.0009693.
M. B. de Lima Barros, T. M. Schubach, M. C. Gutierrez Galhardo, et al., “Sporotrichosis: An Emergent Zoonosis in Rio de Janeiro,” Memórias do Instituto Oswaldo Cruz 96, no. 6 (2001): 777–779, https://doi.org/10.1590/S0074‐02762001000600006.
A. Etchecopaz, M. A. Toscanini, A. Gisbert, et al., “Sporothrix brasiliensis: A Review of an Emerging South American Fungal Pathogen, its Related Disease, Presentation and Spread in Argentina,” Journal of Fungi 7 (2021): 1–33, https://doi.org/10.3390/jof7030170.
P. Thomson, C. González, O. Blank, et al., “Sporotrichosis Outbreak Due to Sporothrix brasiliensis in Domestic Cats in Magallanes, Chile: A One‐Health‐Approach Study,” Journal of Fungi 9 (2023): 226, https://doi.org/10.3390/jof9020226.
F. Almeida‐Silva, V. B. S. Rabello, B. S. Scramignon‐Costa, R. M. Zancopé‐Oliveira, P. M. de Macedo, and R. Almeida‐Paes, “Beyond Domestic Cats: Environmental Detection of Sporothrix brasiliensis DNA in a Hyperendemic Area of Sporotrichosis in Rio de Janeiro State, Brazil,” Journal of Fungi 8 (2022): 604, https://doi.org/10.3390/jof8060604.
R. Marimon, J. Cano, J. Gené, D. A. Sutton, M. Kawasaki, and J. Guarro, “Sporothrix brasiliensis, S. globosa, and S. mexicana, Three New Sporothrix Species of Clinical Interest,” Journal of Clinical Microbiology 45 (2007): 3198–3206, https://doi.org/10.1128/JCM.00808‐07.
B. Spruijtenburg, A. Bombassaro, E. F. J. Meijer, et al., “Sporothrix brasiliensis Genotyping Reveals Numerous Independent Zoonotic Introductions in Brazil,” Journal of Infection 86 (2023): 610–613, https://doi.org/10.1016/j.jinf.2023.02.034.
A. Bombassaro, B. Spruijtenburg, F. Medeiros, et al., “Genotyping and Antifungal Susceptibility Testing of Sporothrix brasiliensis Isolates From Southern Brazil,” Mycoses 66 (2023): 585–593, https://doi.org/10.1111/myc.13584.
L. C. M. L. Losada, R. C. Monteiro, J. A. de Carvalho, et al., “High‐Throughput Microsatellite Markers Development for Genetic Characterization of Emerging Sporothrix Species,” Journal of Fungi 9 (2023): 354, https://doi.org/10.3390/jof9030354.
S. S. Gonçalves, I. da Cruz Bahiense Rocha, B. C. Rediguieri, et al., “Human and Feline Sporotrichosis in a Reference Center of Southeastern Brazil: Genetic Differentiation, Diversity, and Antifungal Susceptibility of Sporothrix Species,” Journal of Fungi 9 (2023): 831, https://doi.org/10.3390/jof9080831.
J. Eudes Filho, I. B. D. Santos, C. M. S. Reis, et al., “A Novel Sporothrix brasiliensis Genomic Variant in Midwestern Brazil: Evidence for an Older and Wider Sporotrichosis Epidemic,” Emerging Microbes & Infections 9 (2020): 2515–2525, https://doi.org/10.1080/22221751.2020.1847001.
V. B. de Souza Rabello, T. M. de Melo, W. Meyer, et al., “Multi‐Locus Sequencing Typing Reveals Geographically Related Intraspecies Variability of Sporothrix brasiliensis,” Fungal Genetics and Biology 170 (2024): 103845, https://doi.org/10.1016/j.fgb.2023.103845.
A. R. dos Santos, E. Misas, B. Min, et al., “Emergence of Zoonotic Sporotrichosis in Brazil: A Genomic Epidemiology Study,” Lancet Microbe 5 (2024): e282–e290, https://doi.org/10.1016/S2666‐5247(23)00364‐6.
M. Teixeira Mde, A. M. Rodrigues, C. K. Tsui, et al., “Asexual Propagation of a Virulent Clone Complex in a Human and Feline Outbreak of Sporotrichosis,” Eukaryotic Cell 14 (2015): 158–169, https://doi.org/10.1128/EC.00153‐14.
M. T. Paiva, C. S. F. de Oliveira, R. R. Nicolino, et al., “Spatial Association Between Sporotrichosis in Cats and in Human During a Brazilian Epidemics,” Preventive Veterinary Medicine 183 (2020): 105125, https://doi.org/10.1016/j.prevetmed.2020.105125.
S. M. Moreira, E. H. P. Andrade, M. T. Paiva, et al., “Implementation of an Animal Sporotrichosis Surveillance and Control Program, Southeastern Brazil,” Emerging Infectious Diseases 27 (2021): 949–952, https://doi.org/10.3201/eid2703.202863.
A. M. Rodrigues, G. S. de Hoog, and Z. P. de Camargo, “Molecular Diagnosis of Pathogenic Sporothrix Species,” Molecular Diagnosis of Pathogenic Sporothrix Species 9 (2015): 1–22, https://doi.org/10.1371/journal.pntd.0004190.
J. A. de Carvalho, F. Hagen, M. C. Fisher, Z. P. de Camargo, and A. M. Rodrigues, “Genome‐Wide Mapping Using New AFLP Markers to Explore Intraspecific Variation Among Pathogenic Sporothrix Species,” PLoS Neglected Tropical Diseases 14, no. 7 (2020): e0008330, https://doi.org/10.1371/journal.pntd.0008330.
P. Jaccard, “The Distribution of the Flora in the Alpine Zone.1,” New Phytologist 11 (1912): 37–50, https://doi.org/10.1111/j.1469‐8137.1912.tb05611.x.
P. R. Hunter and M. A. Gaston, “Numerical Index of the Discriminatory Ability of Typing Systems: An Application of Simpson's Index of Diversity,” Journal of Clinical Microbiology 26 (1988): 2465–2466, https://doi.org/10.1128/jcm.26.11.2465‐2466.1988.
T. Kohonen, “The Self‐Organizing Map,” Proceedings of the IEEE 78 (1990): 1464–1480, https://doi.org/10.1109/5.58325.
J. A. de Carvalho, B. G. Pinheiro, F. Hagen, et al., “A New Duplex PCR Assay for the Rapid Screening of Mating‐Type Idiomorphs of Pathogenic Sporothrix Species,” Fungal Biology 125 (2021): 834–843, https://doi.org/10.1016/j.funbio.2021.05.005.
K. O. Sanchotene, I. M. Madrid, G. B. Klafke, et al., “Sporothrix brasiliensis Outbreaks and the Rapid Emergence of Feline Sporotrichosis,” Mycoses 58, no. 11 (2015): 652–658, https://doi.org/10.1111/myc.12414.
J. S. Boechat, M. M. E. Oliveira, R. Almeida‐Paes, et al., “Feline Sporotrichosis: Associations Between Clinical‐Epidemiological Profiles and Phenotypic‐Genotypic Characteristics of the Etiological Agents in the Rio de Janeiro Epizootic Area,” Memórias do Instituto Oswaldo Cruz 113 (2018): 185–196, https://doi.org/10.1590/0074‐02760170407.
A. M. Rodrigues, G. de Hoog, Y. Zhang, and Z. P. de Camargo, “Emerging Sporotrichosis Is Driven by Clonal and Recombinant Sporothrix Species,” Emerging Microbes & Infections 3, no. 1 (2014): 1–10, https://doi.org/10.1038/emi.2014.33.
P. P. Della Terra, A. M. Rodrigues, G. F. Fernandes, A. S. Nishikaku, E. Burger, and Z. P. de Camargo, “Exploring Virulence and Immunogenicity in the Emerging Pathogen Sporothrix brasiliensis,” PLoS Neglected Tropical Diseases 11 (2017): e0005903, https://doi.org/10.1371/journal.pntd.0005903.
I. D. F. Gremião, E. Martins da Silva da Rocha, H. Montenegro, et al., “Guideline for the Management of Feline Sporotrichosis Caused by Sporothrix brasiliensis and Literature Revision,” Brazilian Journal of Microbiology 52 (2021): 107–124, https://doi.org/10.1007/s42770‐020‐00365‐3.
L. O. Lecca, M. T. Paiva, C. S. F. de Oliveira, et al., “Associated Factors and Spatial Patterns of the Epidemic Sporotrichosis in a High Density Human Populated Area: A Cross‐Sectional Study From 2016 to 2018,” Preventive Veterinary Medicine 176 (2020): 104939, https://doi.org/10.1016/j.prevetmed.2020.104939.
V. C. R. Magalhães, S. A. Colombo, G. J. C. Freitas, et al., “Late Diagnosis of Disseminated Sporothrix brasiliensis Infection With Bone Marrow Involvement in an HIV‐Negative Patient,” Pathogens 11 (2022): 1516, https://doi.org/10.3390/pathogens11121516.
S. Sun, M. A. Coelho, M. David‐Palma, S. J. Priest, and J. Heitman, “The Evolution of Sexual Reproduction and the Mating‐Type Locus: Links to Pathogenesis of Cryptococcus Human Pathogenic Fungi,” Annual Review of Genetics 53 (2019): 417–444, https://doi.org/10.1146/annurev‐genet‐120116‐024755.
I. da Cruz Bahiense Rocha, T. P. P. Della, R. Cardoso de Oliveira, et al., “Molecular‐Based Assessment of Diversity and Population Structure of Sporothrix spp. Clinical Isolates From Espírito Santo‐Brazil,” Mycoses 64 (2021): 420–427, https://doi.org/10.1111/myc.13230.
S. Alvarez‐Perez, J. Blanco, P. Alba, and M. Garcia, “Mating Type and Invasiveness Are Significantly Associated in Aspergillus fumigatus,” Medical Mycology 48 (2009): 1–6, https://doi.org/10.1080/13693780903095414.
M. C. Monteiro, R. Garcia‐Rubio, L. Alcazar‐Fuoli, T. Peláez, and E. Mellado, “Could the Determination of Aspergillus fumigatus Mating Type Have Prognostic Value in Invasive Aspergillosis?” Mycoses 61 (2018): 172–178, https://doi.org/10.1111/myc.12720.
K. Nielsen, R. E. Marra, F. Hagen, et al., “Interaction Between Genetic Background and the Mating‐Type Locus in Cryptococcus neoformans Virulence Potential,” Genetics 171 (2005): 975–983, https://doi.org/10.1534/genetics.105.045039.
K. Nielsen, G. M. Cox, A. P. Litvintseva, et al., “Cryptococcus neoformans α Strains Preferentially Disseminate to the Central Nervous System During Coinfection,” Infection and Immunity 73 (2005): 4922–4933, https://doi.org/10.1128/IAI.73.8.4922‐4933.2005.
K. J. Kwon‐Chung, J. C. Edman, and B. L. Wickes, “Genetic Association of Mating Types and Virulence in Cryptococcus neoformans,” Infection and Immunity 60 (1992): 602–605, https://doi.org/10.1128/iai.60.2.602‐605.1992.