Unravelling the interactions of the environmental host Acanthamoeba castellanii with fungi through the recognition by mannose-binding proteins

Diego de Souza Gonçalves, Marina da Silva Ferreira, Kamilla Xavier Gomes, Claudia Rodríguez-de La Noval, Susie Coutinho Liedke, Giovani Carlo Veríssimo da Costa, Patricia Albuquerque, Juliana Reis Cortines, Regina Helena Saramago Peralta, José Mauro Peralta, Arturo Casadevall, Allan J. Guimarães

Research output: Contribution to journalArticle

Abstract

Free-living amoebae (FLAs) are major reservoirs for a variety of bacteria, viruses, and fungi. The most studied mycophagic FLA, Acanthamoeba castellanii (Ac), is a potential environmental host for endemic fungal pathogens such as Cryptococcus spp., Histoplasma capsulatum, Blastomyces dermatitides, and Sporothrix schenckii. However, the mechanisms involved in this interaction are poorly understood. The aim of this work was to characterize the molecular instances that enable Ac to interact with and ingest fungal pathogens, a process that could lead to selection and maintenance of possible virulence factors. The interaction of Ac with a variety of fungal pathogens was analysed in a multifactorial evaluation that included the role of multiplicity of infection over time. Fungal binding to Ac surface by living image consisted of a quick process, and fungal initial extrusion (vomocytosis) was detected from 15 to 80 min depending on the organism. When these fungi were cocultured with the amoeba, only Candida albicans and Cryptococcus neoformans were able to grow, whereas Paracoccidioides brasiliensis and Sporothrix brasiliensis displayed unchanged viability. Yeasts of H. capsulatum and Saccharomyces cerevisiae were rapidly killed by Ac; however, some cells remained viable after 48 hr. To evaluate changes in fungal virulence upon cocultivation with Ac, recovered yeasts were used to infect Galleria mellonella, and in all instances, they killed the larvae faster than control yeasts. Surface biotinylated extracts of Ac exhibited intense fungal binding by FACS and fluorescence microscopy. Binding was also intense to mannose, and mass spectrometry identified Ac proteins with affinity to fungal surfaces including two putative transmembrane mannose-binding proteins (MBP, L8WXW7 and MBP1, Q6J288). Consistent with interactions with such mannose-binding proteins, Ac-fungi interactions were inhibited by mannose. These MBPs may be involved in fungal recognition by amoeba and promotes interactions that allow the emergence and maintenance of fungal virulence for animals.

Original languageEnglish (US)
Pages (from-to)e13066
JournalCellular microbiology
Volume21
Issue number10
DOIs
StatePublished - Oct 1 2019

Fingerprint

Acanthamoeba castellanii
Mannose-Binding Lectin
Fungi
Amoeba
Sporothrix
Yeasts
Mannose
Virulence
Blastomyces
Maintenance
Paracoccidioides
Histoplasma
Cryptococcus
Cryptococcus neoformans
Virulence Factors
Dermatitis
Coculture Techniques
Candida albicans
Fluorescence Microscopy
Larva

Keywords

  • A. castellanii
  • interaction
  • mannose receptors
  • pathogenic fungi
  • virulence

ASJC Scopus subject areas

  • Microbiology
  • Immunology
  • Virology

Cite this

Gonçalves, D. D. S., Ferreira, M. D. S., Gomes, K. X., Rodríguez-de La Noval, C., Liedke, S. C., da Costa, G. C. V., ... Guimarães, A. J. (2019). Unravelling the interactions of the environmental host Acanthamoeba castellanii with fungi through the recognition by mannose-binding proteins. Cellular microbiology, 21(10), e13066. https://doi.org/10.1111/cmi.13066

Unravelling the interactions of the environmental host Acanthamoeba castellanii with fungi through the recognition by mannose-binding proteins. / Gonçalves, Diego de Souza; Ferreira, Marina da Silva; Gomes, Kamilla Xavier; Rodríguez-de La Noval, Claudia; Liedke, Susie Coutinho; da Costa, Giovani Carlo Veríssimo; Albuquerque, Patricia; Cortines, Juliana Reis; Saramago Peralta, Regina Helena; Peralta, José Mauro; Casadevall, Arturo; Guimarães, Allan J.

In: Cellular microbiology, Vol. 21, No. 10, 01.10.2019, p. e13066.

Research output: Contribution to journalArticle

Gonçalves, DDS, Ferreira, MDS, Gomes, KX, Rodríguez-de La Noval, C, Liedke, SC, da Costa, GCV, Albuquerque, P, Cortines, JR, Saramago Peralta, RH, Peralta, JM, Casadevall, A & Guimarães, AJ 2019, 'Unravelling the interactions of the environmental host Acanthamoeba castellanii with fungi through the recognition by mannose-binding proteins', Cellular microbiology, vol. 21, no. 10, pp. e13066. https://doi.org/10.1111/cmi.13066
Gonçalves, Diego de Souza ; Ferreira, Marina da Silva ; Gomes, Kamilla Xavier ; Rodríguez-de La Noval, Claudia ; Liedke, Susie Coutinho ; da Costa, Giovani Carlo Veríssimo ; Albuquerque, Patricia ; Cortines, Juliana Reis ; Saramago Peralta, Regina Helena ; Peralta, José Mauro ; Casadevall, Arturo ; Guimarães, Allan J. / Unravelling the interactions of the environmental host Acanthamoeba castellanii with fungi through the recognition by mannose-binding proteins. In: Cellular microbiology. 2019 ; Vol. 21, No. 10. pp. e13066.
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