Contact-induced apical asymmetry drives the thigmotropic responses of Candida albicans hyphae

Darren D Thomson, Silvia Wehmeier, FitzRoy J Byfield, Paul A Janmey, David Caballero-Lima, Alison Crossley, Alexandra C Brand

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Abstract

Filamentous hyphae of the human pathogen, Candida albicans, invade mucosal layers and medical silicones. In vitro, hyphal tips re-orient thigmotropically on contact with small obstacles. It is not known how surface topography is sensed but hyphae lacking the cortical marker, Rsr1/Bud1, are unresponsive. We show that, on surfaces, the morphology of hyphal tips and the position of internal polarity-protein complexes are asymmetrically skewed towards the substratum, and biased towards the softer of two surfaces. In nano-fabricated chambers, the Spitzenkörper (Spk) responded to touch by translocating across the apex towards the point of contact, where its stable maintenance correlated with contour-following growth. In the rsr1Δ mutant, the position of the Spk meandered and these responses were attenuated. Perpendicular collision caused lateral Spk oscillation within the tip until after establishment of a new growth axis, suggesting Spk position does not predict the direction of growth in C. albicans. Acute tip re-orientation occurred only in cells where forward growth was countered by hyphal friction sufficient to generate a tip force of ∼ 8.7 μN (1.2 MPa), more than that required to penetrate host-cell membranes. These findings suggest mechanisms through which the organisation of hyphal tip growth in C. albicans facilitates the probing, penetration and invasion of host tissue.

Original languageEnglish
Pages (from-to)342-354
Number of pages13
JournalCellular Microbiology
Volume17
Issue number3
Early online date25 Nov 2014
DOIs
Publication statusPublished - Mar 2015

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Hyphae
Candida albicans
Growth
Friction
Touch
Silicones
Maintenance
Cell Membrane
Drive
Proteins

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Contact-induced apical asymmetry drives the thigmotropic responses of Candida albicans hyphae. / Thomson, Darren D; Wehmeier, Silvia; Byfield, FitzRoy J; Janmey, Paul A; Caballero-Lima, David; Crossley, Alison; Brand, Alexandra C.

In: Cellular Microbiology, Vol. 17, No. 3, 03.2015, p. 342-354.

Research output: Contribution to journalArticle

Thomson, Darren D ; Wehmeier, Silvia ; Byfield, FitzRoy J ; Janmey, Paul A ; Caballero-Lima, David ; Crossley, Alison ; Brand, Alexandra C. / Contact-induced apical asymmetry drives the thigmotropic responses of Candida albicans hyphae. In: Cellular Microbiology. 2015 ; Vol. 17, No. 3. pp. 342-354.
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abstract = "Filamentous hyphae of the human pathogen, Candida albicans, invade mucosal layers and medical silicones. In vitro, hyphal tips re-orient thigmotropically on contact with small obstacles. It is not known how surface topography is sensed but hyphae lacking the cortical marker, Rsr1/Bud1, are unresponsive. We show that, on surfaces, the morphology of hyphal tips and the position of internal polarity-protein complexes are asymmetrically skewed towards the substratum, and biased towards the softer of two surfaces. In nano-fabricated chambers, the Spitzenk{\"o}rper (Spk) responded to touch by translocating across the apex towards the point of contact, where its stable maintenance correlated with contour-following growth. In the rsr1Δ mutant, the position of the Spk meandered and these responses were attenuated. Perpendicular collision caused lateral Spk oscillation within the tip until after establishment of a new growth axis, suggesting Spk position does not predict the direction of growth in C. albicans. Acute tip re-orientation occurred only in cells where forward growth was countered by hyphal friction sufficient to generate a tip force of ∼ 8.7 μN (1.2 MPa), more than that required to penetrate host-cell membranes. These findings suggest mechanisms through which the organisation of hyphal tip growth in C. albicans facilitates the probing, penetration and invasion of host tissue.",
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