Extracellular fibrils of pathogenic yeast Cryptococcus gattii are important for ecological niche, murine virulence and human neutrophil interactions

Deborah J. Springer, Ping Ren, Ramesh Raina, Yimin Dong, Melissa J. Behr, Bruce F. McEwen, Samuel S. Bowser, William A. Samsonoff, Sudha Chaturvedi, Vishnu Chaturvedi

Research output: Contribution to journalArticle

41 Citations (Scopus)

Abstract

Cryptococcus gattii, an emerging fungal pathogen of humans and animals, is found on a variety of trees in tropical and temperate regions. The ecological niche and virulence of this yeast remain poorly defined. We used Arabidopsis thaliana plants and plant-derived substrates to model C. gattii in its natural habitat. Yeast cells readily colonized scratch-wounded plant leaves and formed distinctive extracellular fibrils (40-100 nm diameter ×500-3000 nm length). Extracellular fibrils were observed on live plants and plant-derived substrates by scanning electron microscopy (SEM) and by high voltage-EM (HVEM). Only encapsulated yeast cells formed extracellular fibrils as a capsule-deficient C. gattii mutant completely lacked fibrils. Cells deficient in environmental sensing only formed disorganized extracellular fibrils as apparent from experiments with a C. gattii STE12α mutant. C. gattii cells with extracellular fibrils were more virulent in murine model of pulmonary and systemic cryptococcosis than cells lacking fibrils. C. gattii cells with extracellular fibrils were also significantly more resistant to killing by human polymorphonuclear neutrophils (PMN) in vitro even though these PMN produced elaborate neutrophil extracellular traps (NETs). These observations suggest that extracellular fibril formation could be a structural adaptation of C. gattii for cell-to-cell, cell-to-substrate and/or cell-to-phagocyte communications. Such ecological adaptation of C. gattii could play roles in enhanced virulence in mammalian hosts at least initially via inhibition of host PMN-mediated killing.

Original languageEnglish (US)
Article numbere10978
JournalPLoS One
Volume5
Issue number6
DOIs
StatePublished - 2010
Externally publishedYes

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Cryptococcus gattii
Yeast
Virulence
neutrophils
niches
Neutrophils
virulence
Yeasts
yeasts
mice
Substrates
Cells
Pathogens
cells
Capsules
Animals
Scanning electron microscopy
Communication
Electric potential
Cryptococcosis

ASJC Scopus subject areas

  • Medicine(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Extracellular fibrils of pathogenic yeast Cryptococcus gattii are important for ecological niche, murine virulence and human neutrophil interactions. / Springer, Deborah J.; Ren, Ping; Raina, Ramesh; Dong, Yimin; Behr, Melissa J.; McEwen, Bruce F.; Bowser, Samuel S.; Samsonoff, William A.; Chaturvedi, Sudha; Chaturvedi, Vishnu.

In: PLoS One, Vol. 5, No. 6, e10978, 2010.

Research output: Contribution to journalArticle

Springer, DJ, Ren, P, Raina, R, Dong, Y, Behr, MJ, McEwen, BF, Bowser, SS, Samsonoff, WA, Chaturvedi, S & Chaturvedi, V 2010, 'Extracellular fibrils of pathogenic yeast Cryptococcus gattii are important for ecological niche, murine virulence and human neutrophil interactions', PLoS One, vol. 5, no. 6, e10978. https://doi.org/10.1371/journal.pone.0010978
Springer, Deborah J. ; Ren, Ping ; Raina, Ramesh ; Dong, Yimin ; Behr, Melissa J. ; McEwen, Bruce F. ; Bowser, Samuel S. ; Samsonoff, William A. ; Chaturvedi, Sudha ; Chaturvedi, Vishnu. / Extracellular fibrils of pathogenic yeast Cryptococcus gattii are important for ecological niche, murine virulence and human neutrophil interactions. In: PLoS One. 2010 ; Vol. 5, No. 6.
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