A hidden battle in the dirt: Soil amoebae interactions with Paracoccidioides spp

Detalhes bibliográficos
Autor(a) principal: Albuquerque, Patrícia
Data de Publicação: 2019
Outros Autores: 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
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.
id UNSP_ec491252180128bfb988cac64dbe79b2
oai_identifier_str oai:repositorio.unesp.br:11449/199515
network_acronym_str UNSP
network_name_str Repositório Institucional da UNESP
repository_id_str 2946
spelling 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
_version_ 1799965366018899968