A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp
Autor(a) principal: | |
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Data de Publicação: | 2019 |
Outros Autores: | , , , , , , , , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UNESP |
Texto Completo: | http://dx.doi.org/10.1371/journal.pntd.0007742 http://hdl.handle.net/11449/199515 |
Resumo: | Paracoccidioides spp. are thermodimorphic fungi that cause a neglected tropical disease (paracoccidioidomycosis) that is endemic to Latin America. These fungi inhabit the soil, where they live as saprophytes with no need for a mammalian host to complete their life cycle. Despite this, they developed sophisticated virulence attributes allowing them not only to survive in host tissues but also to cause disease. A hypothesis for selective pressures driving the emergence or maintenance of virulence of soil fungi is their interaction with soil predators such as amoebae and helminths. We evaluated the presence of environmental amoeboid predators in soil from armadillo burrows where Paracoccidioides had been previously detected and tested if the interaction of Paracoccidioides with amoebae selects for fungi with increased virulence. Nematodes, ciliates, and amoebae–all potential predators of fungi–grew in cultures from soil samples. Microscopical observation and ITS sequencing identified the amoebae as Acanthamoeba spp, Allovahlkampfia spelaea, and Vermamoeba vermiformis. These three amoebae efficiently ingested, killed and digested Paracoccidioides spp. yeast cells, as did laboratory adapted axenic Acanthamoeba castellanii. Sequential co-cultivation of Paracoccidioides with A. castellanii selected for phenotypical traits related to the survival of the fungus within a natural predator as well as in murine macrophages and in vivo (Galleria mellonella and mice). These changes in virulence were linked to the accumulation of cell wall alpha-glucans, polysaccharides that mask recognition of fungal molecular patterns by host pattern recognition receptors. Altogether, our results indicate that Paracoccidioides inhabits a complex environment with multiple amoeboid predators that can exert selective pressure to guide the evolution of virulence traits. |
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A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides sppParacoccidioides spp. are thermodimorphic fungi that cause a neglected tropical disease (paracoccidioidomycosis) that is endemic to Latin America. These fungi inhabit the soil, where they live as saprophytes with no need for a mammalian host to complete their life cycle. Despite this, they developed sophisticated virulence attributes allowing them not only to survive in host tissues but also to cause disease. A hypothesis for selective pressures driving the emergence or maintenance of virulence of soil fungi is their interaction with soil predators such as amoebae and helminths. We evaluated the presence of environmental amoeboid predators in soil from armadillo burrows where Paracoccidioides had been previously detected and tested if the interaction of Paracoccidioides with amoebae selects for fungi with increased virulence. Nematodes, ciliates, and amoebae–all potential predators of fungi–grew in cultures from soil samples. Microscopical observation and ITS sequencing identified the amoebae as Acanthamoeba spp, Allovahlkampfia spelaea, and Vermamoeba vermiformis. These three amoebae efficiently ingested, killed and digested Paracoccidioides spp. yeast cells, as did laboratory adapted axenic Acanthamoeba castellanii. Sequential co-cultivation of Paracoccidioides with A. castellanii selected for phenotypical traits related to the survival of the fungus within a natural predator as well as in murine macrophages and in vivo (Galleria mellonella and mice). These changes in virulence were linked to the accumulation of cell wall alpha-glucans, polysaccharides that mask recognition of fungal molecular patterns by host pattern recognition receptors. Altogether, our results indicate that Paracoccidioides inhabits a complex environment with multiple amoeboid predators that can exert selective pressure to guide the evolution of virulence traits.Faculty of Ceilândia University of BrasíliaDepartment of Cell Biology Institute of Biological Sciences University of BrasíliaDepartment of Molecular Microbiology and Immunology Johns Hopkins Bloomberg School of Public HealthFaculty of Medicine University of BrasíliaProgram in Genomic Sciences Catholic University of BrasíliaMilitary CollegeDepartment of Microbiology and Parasitology Biomedical Institute Fluminense Federal UniversityDepartment of Microbiology and Immunology Biosciences Institute UNESPDepartment of Microbiology and Immunology Biosciences Institute UNESPUniversity of BrasíliaJohns Hopkins Bloomberg School of Public HealthCatholic University of BrasíliaMilitary CollegeFluminense Federal UniversityUniversidade Estadual Paulista (Unesp)Albuquerque, PatríciaNicola, André MoraesMagnabosco, Diogo Almeida Gomesda Silveira Derengowski, LorenaCrisóstomo, Luana SoaresXavier, Luciano Costa Gomesde Oliveira Frazão, StefâniaGuilhelmelli, FernandaDe Oliveira, Marco Antôniodo Nascimento Dias, JhonesHurtado, Fabián Andrésde Melo Teixeira, MarcusGuimarães, Allan JeffersonPaes, Hugo CostaBagagli, Eduardo [UNESP]Felipe, Maria Sueli SoaresCasadevall, ArturoSilvaPereira, Ildinete2020-12-12T01:42:02Z2020-12-12T01:42:02Z2019-01-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1371/journal.pntd.0007742PLoS Neglected Tropical Diseases, v. 13, n. 10, 2019.1935-27351935-2727http://hdl.handle.net/11449/19951510.1371/journal.pntd.00077422-s2.0-85073580074Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengPLoS Neglected Tropical Diseasesinfo:eu-repo/semantics/openAccess2021-10-23T07:40:25Zoai:repositorio.unesp.br:11449/199515Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462021-10-23T07:40:25Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false |
dc.title.none.fl_str_mv |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp |
title |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp |
spellingShingle |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp Albuquerque, Patrícia |
title_short |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp |
title_full |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp |
title_fullStr |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp |
title_full_unstemmed |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp |
title_sort |
A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp |
author |
Albuquerque, Patrícia |
author_facet |
Albuquerque, Patrícia Nicola, André Moraes Magnabosco, Diogo Almeida Gomes da Silveira Derengowski, Lorena Crisóstomo, Luana Soares Xavier, Luciano Costa Gomes de Oliveira Frazão, Stefânia Guilhelmelli, Fernanda De Oliveira, Marco Antônio do Nascimento Dias, Jhones Hurtado, Fabián Andrés de Melo Teixeira, Marcus Guimarães, Allan Jefferson Paes, Hugo Costa Bagagli, Eduardo [UNESP] Felipe, Maria Sueli Soares Casadevall, Arturo SilvaPereira, Ildinete |
author_role |
author |
author2 |
Nicola, André Moraes Magnabosco, Diogo Almeida Gomes da Silveira Derengowski, Lorena Crisóstomo, Luana Soares Xavier, Luciano Costa Gomes de Oliveira Frazão, Stefânia Guilhelmelli, Fernanda De Oliveira, Marco Antônio do Nascimento Dias, Jhones Hurtado, Fabián Andrés de Melo Teixeira, Marcus Guimarães, Allan Jefferson Paes, Hugo Costa Bagagli, Eduardo [UNESP] Felipe, Maria Sueli Soares Casadevall, Arturo SilvaPereira, Ildinete |
author2_role |
author author author author author author author author author author author author author author author author author |
dc.contributor.none.fl_str_mv |
University of Brasília Johns Hopkins Bloomberg School of Public Health Catholic University of Brasília Military College Fluminense Federal University Universidade Estadual Paulista (Unesp) |
dc.contributor.author.fl_str_mv |
Albuquerque, Patrícia Nicola, André Moraes Magnabosco, Diogo Almeida Gomes da Silveira Derengowski, Lorena Crisóstomo, Luana Soares Xavier, Luciano Costa Gomes de Oliveira Frazão, Stefânia Guilhelmelli, Fernanda De Oliveira, Marco Antônio do Nascimento Dias, Jhones Hurtado, Fabián Andrés de Melo Teixeira, Marcus Guimarães, Allan Jefferson Paes, Hugo Costa Bagagli, Eduardo [UNESP] Felipe, Maria Sueli Soares Casadevall, Arturo SilvaPereira, Ildinete |
description |
Paracoccidioides spp. are thermodimorphic fungi that cause a neglected tropical disease (paracoccidioidomycosis) that is endemic to Latin America. These fungi inhabit the soil, where they live as saprophytes with no need for a mammalian host to complete their life cycle. Despite this, they developed sophisticated virulence attributes allowing them not only to survive in host tissues but also to cause disease. A hypothesis for selective pressures driving the emergence or maintenance of virulence of soil fungi is their interaction with soil predators such as amoebae and helminths. We evaluated the presence of environmental amoeboid predators in soil from armadillo burrows where Paracoccidioides had been previously detected and tested if the interaction of Paracoccidioides with amoebae selects for fungi with increased virulence. Nematodes, ciliates, and amoebae–all potential predators of fungi–grew in cultures from soil samples. Microscopical observation and ITS sequencing identified the amoebae as Acanthamoeba spp, Allovahlkampfia spelaea, and Vermamoeba vermiformis. These three amoebae efficiently ingested, killed and digested Paracoccidioides spp. yeast cells, as did laboratory adapted axenic Acanthamoeba castellanii. Sequential co-cultivation of Paracoccidioides with A. castellanii selected for phenotypical traits related to the survival of the fungus within a natural predator as well as in murine macrophages and in vivo (Galleria mellonella and mice). These changes in virulence were linked to the accumulation of cell wall alpha-glucans, polysaccharides that mask recognition of fungal molecular patterns by host pattern recognition receptors. Altogether, our results indicate that Paracoccidioides inhabits a complex environment with multiple amoeboid predators that can exert selective pressure to guide the evolution of virulence traits. |
publishDate |
2019 |
dc.date.none.fl_str_mv |
2019-01-01 2020-12-12T01:42:02Z 2020-12-12T01:42:02Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://dx.doi.org/10.1371/journal.pntd.0007742 PLoS Neglected Tropical Diseases, v. 13, n. 10, 2019. 1935-2735 1935-2727 http://hdl.handle.net/11449/199515 10.1371/journal.pntd.0007742 2-s2.0-85073580074 |
url |
http://dx.doi.org/10.1371/journal.pntd.0007742 http://hdl.handle.net/11449/199515 |
identifier_str_mv |
PLoS Neglected Tropical Diseases, v. 13, n. 10, 2019. 1935-2735 1935-2727 10.1371/journal.pntd.0007742 2-s2.0-85073580074 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
PLoS Neglected Tropical Diseases |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.source.none.fl_str_mv |
Scopus reponame:Repositório Institucional da UNESP instname:Universidade Estadual Paulista (UNESP) instacron:UNESP |
instname_str |
Universidade Estadual Paulista (UNESP) |
instacron_str |
UNESP |
institution |
UNESP |
reponame_str |
Repositório Institucional da UNESP |
collection |
Repositório Institucional da UNESP |
repository.name.fl_str_mv |
Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP) |
repository.mail.fl_str_mv |
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1799965366018899968 |