Paracoccidioides restrepiensis has undergone a severe population bottleneck
PDF

How to Cite

McEwen, J. G. ., Gómez, O. M. ., & Matute, D. R. . (2022). Paracoccidioides restrepiensis has undergone a severe population bottleneck. Revista De La Academia Colombiana De Ciencias Exactas, Físicas Y Naturales, 46(181), 866–876. https://doi.org/10.18257/raccefyn.1768

Downloads

Download data is not yet available.

Métricas Alternativas


Dimensions

Abstract

Genus Paracoccidioides now encompasses five species, P. lutzii, P. brasiliensis sensu stricto, P. americana, P. venezuelensis, and P. restrepiensis. All the paracoccidioidomycosis (PCM) cases reported in Colombia have been classified as P. restrepiensis, which was named in honor of Angela Restrepo, a leading researcher in the field of the biology of the fungus. Previous assessments of genetic diversity have suggested that Paracoccidioides species have differences in their level of polymorphism. To infer changes in effective population size, we used the Pairwise sequentially Markovian coalescent (PSMC) by generating two pseudodiploids for P. restrepiensis and one for P. brasiliensis sensu stricto. We found that P. restrepiensis diverged from its sister species recently, the divergence time from P. venezuelensis being 125,000 (± 42,000) years. The analyses using PSMC show a systematic reduction in the effective population size of P. restrepiensis with a rapid decrease in genetic variability compared to P. brasiliensis sensu stricto, which indicates that P. restrepiensis has undergone a systematic population bottleneck. None of the other two species show the dramatic effective population size reduction observed in P. restrepiensis. These comparisons suggest that the trajectory of P. restrepiensis is somehow different from the other Paracoccidioides species and poses the question regarding the biogeographic events that have led to such a dramatic population pattern.

https://doi.org/10.18257/raccefyn.1768

Keywords

Paracoccidioides spp. | Paracoccidioides restrepiensis | Paracoccidioidomycosis | Effective population size
PDF

References

Almeida, F. P. (1930). Estudos comparativos do granuloma coccidióidico nos Estados Unidos e no Brasil. Novo gênero para o parasito brasileiro. Annals Faculdade de Medicina Sao Paulo 5, 125-141.

Assolini, J. P., Lenhard-Vidal, A., Bredt, C. S. O., Tano, Z. N., Sano, A., Cezar-Dos-Santos, F., Ono, M. A., Itano, E. N. (2021). Distinct Pattern of Paracoccidioides lutzii, P. restrepiensis and P. americana Antigens Recognized by IgE in Human Paracoccidioidomycosis. Current Microbiology, 78(7), 2608-2614. https://doi.org/10.1007/s00284-021-02508-7

Bagagli, E., Matute, D. R., Garces, H. G., Tenorio, B. G., Garces, A. G., Alves, L. G. B., Yamauchi, D. H., Hrycyk, M. F., Barker, B. M., Teixeira, M. M. (2021). Paracoccidioides brasiliensis Isolated from Nine-Banded Armadillos (Dasypus novemcinctus) Reveal Population Structure and Admixture in the Amazon Basin. Journal of Fungi (Basel), 7(1). https://doi.org/10.3390/jof7010054

Bazzicalupo, E., Lucena-Pérez, M., Kleinman-Ruiz, D., Pavlov, A., Trajçe, A., Hoxha, B., Sanaja, B., Gurielidze, Z., Kerdikoshvili, N., Mamuchadze, J., Yarovenko, Y. A., Akkiev, M. I., Ratkiewicz, M., Saveljev, A. P., Melovski, D., Gavashelishvili, A., Schmidt, K., Godoy, J. A. (2022). History, demography and genetic status of Balkan and Caucasian Lynx lynx (Linnaeus, 1758) populations revealed by genome-wide variation. Diversity and Distributions, 28(1), 65-82. https://doi.org/https://doi.org/10.1111/ddi.13439

Bellissimo-Rodrigues, F., Machado, A. A., Martinez, R. (2011). Paracoccidioidomycosis epidemiological features of a 1,000-cases series from a hyperendemic area on the southeast of Brazil. The American Journal of Tropical Medicine and Hygiene, 85(3), 546-550. https://doi.org/10.4269/ajtmh.2011.11-0084

Cocio, T.A., Nascimento, E., Kress, M., Bagagli, E., Martinez, R. (2020). Characterization of a Paracoccidioides spp. strain from southeastern Brazil genotyped as Paracoccidioides restrepiensis (PS3) and review of this phylogenetic species. Genetics and Molecular Biology, 43(2), e20190201. https://doi.org/10.1590/1678-4685-GMB-2019-0201

Coutinho, Z.F., Wanke, B., Travassos, C., Oliveira, R.M., Xavier, D.R., Coimbra, C. E., Jr. (2015). Hospital morbidity due to paracoccidioidomycosis in Brazil (1998-2006). Tropical Medicine and Intternational Health, 20(5), 673-680. https://doi.org/10.1111/tmi.12472

Dagilis, A.J., Peede, D., Coughlan, J.M., Jofre, G.I., D’Agostino, E.R.R., Mavengere, H., Tate, A.D., Matute, D.R. (2022). A need for standardized reporting of introgression: Insights from studies across eukaryotes. Evolution Letters, n/a(n/a). https://doi.org/https://doi.org/10.1002/evl3.294

DePristo, M.A., Banks, E., Poplin, R., Garimella, K.V., Maguire, J.R., Hartl, C., Philippakis, A.A., del Angel, G., Rivas, M.A., Hanna, M., McKenna, A., Fennell, T.J., Kernytsky, A.M., Sivachenko, A.Y., Cibulskis, K., Gabriel, S.B., Altshuler, D., Daly, M.J. (2011). A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics, 43(5), 491-498. https://doi.org/10.1038/ng.806

Desjardins, C.A., Champion, M.D., Holder, J.W., Muszewska, A., Goldberg, J., Bailao, A.M., Brigido, M.M., Ferreira, M.E., Garcia, A.M., Grynberg, M., Gujja, S., Heiman, D.I., Henn, M.R., Kodira, C.D., Leon-Narvaez, H., Longo, L.V., Ma, L.J., Malavazi, I., Matsuo, A.L., . . . Cuomo, C. A. (2011). Comparative genomic analysis of human fungal pathogens causing paracoccidioidomycosis. PLoS Genetics, 7(10), e1002345. https://doi.org/10.1371/journal.pgen.1002345

Farlow, A., Long, H., Arnoux, S., Sung, W., Doak, T.G., Nordborg, M., Lynch, M. (2015). The Spontaneous Mutation Rate in the Fission Yeast Schizosaccharomyces pombe. Genetics, 201(2), 737-744. https://doi.org/10.1534/genetics.115.177329

Franco, M.F., Del Negro, G., Lacaz, C.d.S., Restrepo-Moreno, A. (1994). Paracoccidioidomycosis. CRC Press. Gao, Z., Przeworski, M., Sella, G. (2015). Footprints of ancient-balanced polymorphisms in genetic variation data from closely related species. Evolution, 69(2), 431-446. https://doi.org/10.1111/evo.12567

Guerrero, R.F., Hahn, M.W. (2018). Quantifying the risk of hemiplasy in phylogenetic inference. Proceedings of the National Academy of Sciences USA, 115(50), 12787-12792. https://doi.org/10.1073/pnas.1811268115

Hamlin, J.A.P., Hibbins, M.S., Moyle, L.C. (2020). Assessing biological factors affecting postspeciation introgression. Evolution Letters, 4(2), 137-154. https://doi.org/10.1002/evl3.159

Lacaz Cda, S., Vidal, M.S., Pereira, C.N., Heins-Vaccari, E.M., de Melo, N.T., Sakai-Valente, N., Arriagada, G.L. (1997). Paracoccidioides cerebriformis Moore, 1935. Mycologic and immunochemical study. Rev Inst Med Trop Sao Paulo, 39(3), 141-144. https://doi.org/10.1590/s0036-46651997000300003

Leffler, E.M., Bullaughey, K., Matute, D.R., Meyer, W.K., Segurel, L., Venkat, A., Andolfatto, P., Przeworski, M. (2012). Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biology, 10(9), e1001388. https://doi.org/10.1371/journal.pbio.1001388

Li, H., Durbin, R. (2011). Inference of human population history from individual whole-genome sequences. Nature, 475(7357), 493-496. https://doi.org/10.1038/nature10231

Lutz, A. (1908). Uma mycose pseudo-coccidica localizada na boca e observada no Brazil: contribuicao ao conhecimento das hyphoblastomycoses americanas. Brasil Medico, 22, 121-124, 141-144.

Lutz, A. (2004). Lutz A Obra completa Uma micose pseudococcídica localizada na boca e observada no Brasil. Contribuição ao conhecimento das hifoblastomicoses americanas.

Fiocruz Lynch, M., Sung, W., Morris, K., Coffey, N., Landry, C.R., Dopman, E. B., Dickinson, W.J., Okamoto, K., Kulkarni, S., Hartl, D.L., Thomas, W.K. (2008). A genome-wide view of the spectrum of spontaneous mutations in yeast. Proceedings of the National Academy of Sciences USA, 105(27), 9272-9277. https://doi.org/10.1073. pnas.0803466105

Mattos, K., Cocio, T. A., Chaves, E. G. A., Borges, C.L., Venturini, J., de Carvalho, L.R., Mendes, R.P., Paniago, A.M.M., Weber, S.S. (2021). An update on the occurrence of Paracoccidioides species in the Midwest region, Brazil: Molecular epidemiology, clinical aspects and serological profile of patients from Mato Grosso do Sul State. PLoS Neglected Tropical Diseases, 15(4), e0009317. https://doi.org/10.1371/journal.pntd.0009317

Matute, D.R., McEwen, J.G., Puccia, R., Montes, B.A., San-Blas, G., Bagagli, E., Rauscher, J.T., Restrepo, A., Morais, F., Nino-Vega, G., Taylor, J.W. (2006). Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Molecular Biology and Evolution, 23(1), 65-73. https://doi.org/10.1093/molbev/msj008

Matute, D.R., Sepulveda, V.E. (2019). Fungal species boundaries in the genomics era. Fungal Genetics and Biology, 131, 103249. https://doi.org/10.1016/j.fgb.2019.103249

Matute, D.R., Sepulveda, V.E., Quesada, L.M., Goldman, G.H., Taylor, J.W., Restrepo, A., McEwen, J.G. (2006). Microsatellite analysis of three phylogenetic species of Paracoccidioides brasiliensis. Journal of Clinical Microbiology, 44(6), 2153-2157. https://doi.org/10.1128/JCM.02540-05

Matute, D.R., Torres, I.P., Salgado-Salazar, C., Restrepo, A., McEwen, J.G. (2007). Background selection at the chitin synthase II (chs2) locus in Paracoccidioides brasiliensis species complex. Fungal Genetics and Biology, 44(5), 357-367. https://doi.org/10.1016/j.fgb.2007.01.006

Mavengere, H., Mattox, K., Teixeira, M.M., Sepulveda, V.E., Gomez, O.M., Hernandez, O., McEwen, J., Matute, D.R. (2020). Paracoccidioides Genomes Reflect High Levels of Species Divergence and Little Interspecific Gene Flow. mBio, 11(6), e01999-01920. https://doi.org/10.1128/mBio.01999-20

Maxwell, C.S., Mattox, K., Turissini, D.A., Teixeira, M.M., Barker, B.M., Matute, D.R. (2019). Gene exchange between two divergent species of the fungal human pathogen, Coccidioides. Evolution, 73(1), 42-58. https://doi.org/10.1111/evo.13643

McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., DePristo, M.A. (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20(9), 1297-1303. https://doi.org/10.1101/gr.107524.110

Morais, F.V., Barros, T.F., Fukada, M.K., Cisalpino, P.S., Puccia, R. (2000). Polymorphism in the gene coding for the immunodominant antigen gp43 from the pathogenic fungus paracoccidioides brasiliensis. Journal of Clinical Microbiology, 38(11), 3960-3966. http://jcm.asm.org/cgi/content/abstract/38/11/3960

Muñoz, J.F., Farrer, R.A., Desjardins, C.A., Gallo, J.E., Sykes, S., Sakthikumar, S., Misas, E., Whiston, E.A., Bagagli, E., Soares, C.M., Teixeira, M.M., Taylor, J. W., Clay, O.K., McEwen, J.G., Cuomo, C.A. (2016). Genome Diversity, Recombination, and Virulence across the Major Lineages of Paracoccidioides. mSphere, 1(5), e00213-00216. https://doi.org/10.1128/mSphere.00213-16

Niño-Vega, G.A., Calcagno, A.M., San-Blas, G., San-Blas, F., Gooday, G.W., & Gow, N.A. (2000). RFLP analysis reveals marked geographical isolation between strains of Paracoccidioides brasiliensis. Medical Mycology, 38(6), 437-441. https://doi.org/10.1080/mmy.38.6.437.441

PAHO, (1971). Paracoccidioidomycosis. Proceedings of the First Pan American Symposium, Medellin, Colombia, Medellín, Colombia.

Restrepo, A. (2000). Morphological aspects of Paracoccidioides brasiliensis in lymph nodes: implications for the prolonged latency of paracoccidioidomycosis?. Medical Mycology, 38(4), 317-322. https://doi.org/10.1080/mmy.38.4.317.322

Restrepo, A., Arango, M. D. (1980). In vitro susceptibility testing of Paracoccidioides brasiliensis to sulfonamides. Antimicrobial Agents and Chemotherapy, 18(1), 190-194. http://www.ncbi.nlm.nih.gov/pubmed/7416744

Restrepo-Moreno, A., Tobon-Orozco, A.M., González-Marín, A. (2020). Paracoccidioidomycosis. In J. E. Bennett, R. Dolin, & M. J. Blaser (Eds.), Mandell, Douglas, and Bennett’s principles and practice of infectious diseases (Ninth edition. ed., Vol. 2, pp. 3211-3221).Elsevier.

Sato, Y., Ogden, R., Kishida, T., Nakajima, N., Maeda, T., Inoue-Murayama, M. (2020). Population history of the golden eagle inferred from whole-genome sequencing of three of its subspecies. Biological Journal of the Linnean Society, 130(4), 826-838. https://doi.org/10.1093/biolinnean/blaa068

Schön, I., Martens, K., Dijk, P.V. (2009). Lost sex: the evolutionary biology of parthenogenesis. Springer.

Scorzoni, L., de Lucas, M.P., Singulani, J.L., de Oliveira, H.C., Assato, P.A., Fusco-Almeida, A.M., Mendes-Giannini, M.J.S. (2018). Evaluation of Caenorhabditis elegans as a host model for Paracoccidioides brasiliensis and Paracoccidioides lutzii. Pathogens and Disease, 76(1). https://doi.org/10.1093/femspd/fty004

Siqueira, I.M., Fraga, C.L., Amaral, A.C., Souza, A.C., Jeronimo, M.S., Correa, J.R., Magalhaes, K.G., Inacio, C.A., Ribeiro, A.M., Burguel, P.H., Felipe, M.S., Tavares, A.H., Bocca, A.L. (2016). Distinct patterns of yeast cell morphology and host responses induced by representative strains of Paracoccidioides brasiliensis (Pb18) and Paracoccidioides lutzii (Pb01). Medical Mycology, 54(2), 177-188. https://doi.org/10.1093/mmy/myv072

Soares, C., Madlun, E., da Silva, S., Pereira, M., Felipe, M. (1995). Characterization of Paracoccidioides brasiliensis isolates by random amplified polymorphic DNA analysis. Journal of Clinical Microbiology, 33(2), 505-507. https://doi.org/10.1128/jcm.33.2.505-507.1995

Splendore, A. (1912). Zymonematosi con localizzazione nella cavita della bocca, osservata in Brasile. Bulletin de la Société de Pathologie Exotique, 5, 313–319.

Taylor, J. W., Branco, S., Gao, C., Hann-Soden, C., Montoya, L., Sylvain, I., Gladieux, P. (2017). Sources of Fungal Genetic Variation and Associating It with Phenotypic Diversity. Microbiology Spectrum, 5(5). https://doi.org/10.1128/microbiolspec.FUNK-0057-2016

Teixeira Mde, M., Theodoro, R.C., Oliveira, F.F., Machado, G.C., Hahn, R.C., Bagagli, E., San-Blas, G., Soares Felipe, M.S. (2014). Paracoccidioides lutzii sp. nov.: biological and clinical implications. Medical Mycology, 52(1), 19-28. https://doi.org/10.3109/13693786.2013.794311

Teixeira, M.M., Cattana, M.E., Matute, D.R., Munoz, J.F., Arechavala, A., Isbell, K., Schipper, R., Santiso, G., Tracogna, F., Sosa, M. L. A., Cech, N., Alvarado, P., Barreto, L., Chacon, Y., Ortellado, J., Lima, C. M., Chang, M. R., Nino-Vega, G., Yasuda, M.A.S., . . . Giusiano, G. (2020). Genomic diversity of the human pathogen Paracoccidioides across the South American continent. Fungal Genetics and Biology, 140, 103395. https://doi.org/10.1016/j.fgb.2020.103395

Teixeira, M.M., Theodoro, R.C., de Carvalho, M. J., Fernandes, L., Paes, H.C., Hahn, R.C., Mendoza, L., Bagagli, E., San-Blas, G., Felipe, M.S. (2009). Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus [Research Support, Non-U.S. Gov’t]. Mol Phylogenet Evol, 52(2), 273-283. https://doi.org/10.1016/j.ympev.2009.04.005

Teixeira, M.M., Theodoro, R.C., Nino-Vega, G., Bagagli, E., Felipe, M.S. (2014). Paracoccidioides species complex: ecology, phylogeny, sexual reproduction, and virulence. PLoS Pathogens, 10(10), e1004397. https://doi.org/10.1371/journal.ppat.1004397

Turissini, D.A., Gómez, O.M., Teixeira, M.M., McEwen, J.G., Matute, D.R. (2017). Species boundaries in the human pathogen Paracoccidioides. Fungal Genetics and Biology, 106, 9-25. https://doi.org/10.1016/j.fgb.2017.05.007

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Copyright (c) 2022 Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales