The fungivorous amoeba Protostelium aurantium targets redox homeostasis and cell wall integrity during intracellular killing of Candida parapsilosis.


Journal

Cellular microbiology
ISSN: 1462-5822
Titre abrégé: Cell Microbiol
Pays: India
ID NLM: 100883691

Informations de publication

Date de publication:
11 2021
Historique:
revised: 08 03 2021
received: 15 07 2019
accepted: 26 08 2021
pubmed: 31 8 2021
medline: 14 1 2022
entrez: 30 8 2021
Statut: ppublish

Résumé

Predatory interactions among microbes are major evolutionary driving forces for biodiversity. The fungivorous amoeba Protostelium aurantium has a wide fungal food spectrum including foremost pathogenic members of the genus Candida. Here we show that upon phagocytic ingestion by the amoeba, Candida parapsilosis is confronted with an oxidative burst and undergoes lysis within minutes of processing in acidified phagolysosomes. On the fungal side, a functional genomic approach identified copper and redox homeostasis as primary targets of amoeba predation, with the highly expressed copper exporter gene CRP1 and the peroxiredoxin gene PRX1 contributing to survival when encountered with P. aurantium. The fungicidal activity was largely retained in intracellular vesicles of the amoebae. Following their isolation, the content of these vesicles induced immediate killing and lysis of C. parapsilosis in vitro. Proteomic analysis identified 56 vesicular proteins from P. aurantium. Although completely unknown proteins were dominant, many of them could be categorised as hydrolytic enzymes targeting the fungal cell wall, indicating that fungal cell wall structures are under selection pressure by predatory phagocytes in natural environments. TAKE AWAY: The amoeba Protostelium aurantium feeds on fungi, such as Candida parapsilosis. Ingested yeast cells are exposed to reactive oxygen species. A copper exporter and a peroxiredoxin contribute to fungal defence. Yeast cells undergo intracellular lysis. Lysis occurs via a cocktail of hydrolytic enzymes from intracellular vesicles.

Identifiants

pubmed: 34460149
doi: 10.1111/cmi.13389
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13389

Subventions

Organisme : Gazdaságfejlesztési és Innovációs Operatív Program
ID : GINOP-2.3.2-15-2016-00035
Organisme : Gazdaságfejlesztési és Innovációs Operatív Program
ID : GINOP-2.3.3-15-2016-00006
Organisme : Deutscher Akademischer Austausch Dienst
Organisme : European Social Fund ESF "Europe for Thuringia"
ID : 2016FGR0053
Organisme : National Research, Development and Innovation Office Hungary
ID : NKFIH K123952
Organisme : German Academic Exchange Service
Organisme : European Social Fund
Organisme : Research Foundation
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2051 - Project-ID 390713860
Organisme : Deutsche Forschungsgemeinschaft
ID : HI 1574/2-1
Organisme : Deutsche Forschungsgemeinschaft
ID : HI 1574/4-1
Organisme : Deutsche Forschungsgemeinschaft
ID : Hu 528/17-1
Organisme : Deutsche Forschungsgemeinschaft
ID : Hu 528/21-1
Organisme : Deutsche Forschungsgemeinschaft
ID : TRR 124 FungiNet

Informations de copyright

© 2021 John Wiley & Sons Ltd.

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Auteurs

Silvia Radosa (S)

Junior Research Group Evolution of Microbial Interactions, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Jakob L Sprague (JL)

Junior Research Group Evolution of Microbial Interactions, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.
Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany.
Department of Microbial Pathogenicity Mechanisms, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Siu-Hin Lau (SH)

Junior Research Group Evolution of Microbial Interactions, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.
Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany.

Renáta Tóth (R)

Department of Microbiology, University of Szeged, Szeged, Hungary.

Jörg Linde (J)

Research Group Systems Biology and Bioinformatics, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Thomas Krüger (T)

Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Marcel Sprenger (M)

Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany.
Department of Microbial Pathogenicity Mechanisms, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Lydia Kasper (L)

Department of Microbial Pathogenicity Mechanisms, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Martin Westermann (M)

Electron Microscopy Center, Jena University Hospital, Jena, Germany.

Olaf Kniemeyer (O)

Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Bernhard Hube (B)

Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany.
Department of Microbial Pathogenicity Mechanisms, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Axel A Brakhage (AA)

Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany.
Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

Attila Gácser (A)

Department of Microbiology, University of Szeged, Szeged, Hungary.

Falk Hillmann (F)

Junior Research Group Evolution of Microbial Interactions, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute (HKI), Jena, Germany.

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