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The two-component sensor kinase TcsC and its role in stress resistance of the human-pathogenic mold Aspergillus fumigatus.

McCormick A, Jacobsen ID, Broniszewska M, Beck J, Heesemann J, Ebel F - PLoS ONE (2012)

Bottom Line: Both hyperosmotic stress and treatment with fludioxonil result in a TcsC-dependent phosphorylation of SakA, the final MAP kinase in the high osmolarity glycerol (HOG) pathway, confirming a role for TcsC in this signaling pathway.Several types of stress, such as hypoxia, exposure to farnesol or elevated concentrations of certain divalent cations, trigger a differentiation in A. fumigatus toward a "fluffy" growth phenotype resulting in white, dome-shaped colonies.Although TcsC plays a role in the adaptation of A. fumigatus to hypoxia, it seems to be dispensable for virulence.

View Article: PubMed Central - PubMed

Affiliation: Max-von-Pettenkofer-Institut, Ludwig-Maximilians-University, Munich, Germany.

ABSTRACT
Two-component signaling systems are widespread in bacteria, but also found in fungi. In this study, we have characterized TcsC, the only Group III two-component sensor kinase of Aspergillus fumigatus. TcsC is required for growth under hyperosmotic stress, but dispensable for normal growth, sporulation and conidial viability. A characteristic feature of the ΔtcsC mutant is its resistance to certain fungicides, like fludioxonil. Both hyperosmotic stress and treatment with fludioxonil result in a TcsC-dependent phosphorylation of SakA, the final MAP kinase in the high osmolarity glycerol (HOG) pathway, confirming a role for TcsC in this signaling pathway. In wild type cells fludioxonil induces a TcsC-dependent swelling and a complete, but reversible block of growth and cytokinesis. Several types of stress, such as hypoxia, exposure to farnesol or elevated concentrations of certain divalent cations, trigger a differentiation in A. fumigatus toward a "fluffy" growth phenotype resulting in white, dome-shaped colonies. The ΔtcsC mutant is clearly more susceptible to these morphogenetic changes suggesting that TcsC normally antagonizes this process. Although TcsC plays a role in the adaptation of A. fumigatus to hypoxia, it seems to be dispensable for virulence.

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The role of TcsC in the stress-induced developmental program leading to a fluffy growth phenotype.Drop dilution assays were performed on AMM plates (supplemented with ammonium). Panel A: 1% oxygen; B: 2% oxygen; C: 2 mM farnesol; D: 200 µM farnesol; E: 2 mM farnesol; F: 100 mM MgSO4; G: 100 mM CaCl2; H: 100 mM MgSO4; I: 50 mM CaCl2; J: 500 mM CaCl2. Side views of colonies from C and D are shown in panels E and F. The depicted colonies were photographed after 48 h at 37°C. AfS35 (top/left); ΔtcsC (middle); complemented strain (bottom/right).
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pone-0038262-g005: The role of TcsC in the stress-induced developmental program leading to a fluffy growth phenotype.Drop dilution assays were performed on AMM plates (supplemented with ammonium). Panel A: 1% oxygen; B: 2% oxygen; C: 2 mM farnesol; D: 200 µM farnesol; E: 2 mM farnesol; F: 100 mM MgSO4; G: 100 mM CaCl2; H: 100 mM MgSO4; I: 50 mM CaCl2; J: 500 mM CaCl2. Side views of colonies from C and D are shown in panels E and F. The depicted colonies were photographed after 48 h at 37°C. AfS35 (top/left); ΔtcsC (middle); complemented strain (bottom/right).

Mentions: Tco1, the Group III HHK of Cryptococcus neoformans, is required for growth under hypoxic conditions [18]. Oxygen limitation is also encountered by A. fumigatus during infection and it was recently shown that its ability to grow under hypoxic conditions is a prerequisite for virulence [19]. Adaptation of A. fumigatus to 1% oxygen results in colonies that are characterized by a massive production of aerial hyphae, resulting in a dome-shaped morphology, and a complete lack of sporulation (Figure 5A). At 1% oxygen the ΔtcsC mutant was indistinguishable from the control strains with respect to growth and colony morphology. At 2% oxygen flat and sporulating colonies were found for the control strains, whereas the mutant colonies remained white and dome-shaped (Fig. 5B). Similar A. nidulans colonies, also characterized by the formation of abundant aerial hyphae and the lack of sporulation, were described previously as having a ‘fluffy’ developmental phenotype [20]. Thus, oxygen limitation seems to activate a specific morphogenetic program and the threshold level of hypoxic stress required to trigger this developmental process is clearly lower in the ΔtcsC mutant.


The two-component sensor kinase TcsC and its role in stress resistance of the human-pathogenic mold Aspergillus fumigatus.

McCormick A, Jacobsen ID, Broniszewska M, Beck J, Heesemann J, Ebel F - PLoS ONE (2012)

The role of TcsC in the stress-induced developmental program leading to a fluffy growth phenotype.Drop dilution assays were performed on AMM plates (supplemented with ammonium). Panel A: 1% oxygen; B: 2% oxygen; C: 2 mM farnesol; D: 200 µM farnesol; E: 2 mM farnesol; F: 100 mM MgSO4; G: 100 mM CaCl2; H: 100 mM MgSO4; I: 50 mM CaCl2; J: 500 mM CaCl2. Side views of colonies from C and D are shown in panels E and F. The depicted colonies were photographed after 48 h at 37°C. AfS35 (top/left); ΔtcsC (middle); complemented strain (bottom/right).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3366943&req=5

pone-0038262-g005: The role of TcsC in the stress-induced developmental program leading to a fluffy growth phenotype.Drop dilution assays were performed on AMM plates (supplemented with ammonium). Panel A: 1% oxygen; B: 2% oxygen; C: 2 mM farnesol; D: 200 µM farnesol; E: 2 mM farnesol; F: 100 mM MgSO4; G: 100 mM CaCl2; H: 100 mM MgSO4; I: 50 mM CaCl2; J: 500 mM CaCl2. Side views of colonies from C and D are shown in panels E and F. The depicted colonies were photographed after 48 h at 37°C. AfS35 (top/left); ΔtcsC (middle); complemented strain (bottom/right).
Mentions: Tco1, the Group III HHK of Cryptococcus neoformans, is required for growth under hypoxic conditions [18]. Oxygen limitation is also encountered by A. fumigatus during infection and it was recently shown that its ability to grow under hypoxic conditions is a prerequisite for virulence [19]. Adaptation of A. fumigatus to 1% oxygen results in colonies that are characterized by a massive production of aerial hyphae, resulting in a dome-shaped morphology, and a complete lack of sporulation (Figure 5A). At 1% oxygen the ΔtcsC mutant was indistinguishable from the control strains with respect to growth and colony morphology. At 2% oxygen flat and sporulating colonies were found for the control strains, whereas the mutant colonies remained white and dome-shaped (Fig. 5B). Similar A. nidulans colonies, also characterized by the formation of abundant aerial hyphae and the lack of sporulation, were described previously as having a ‘fluffy’ developmental phenotype [20]. Thus, oxygen limitation seems to activate a specific morphogenetic program and the threshold level of hypoxic stress required to trigger this developmental process is clearly lower in the ΔtcsC mutant.

Bottom Line: Both hyperosmotic stress and treatment with fludioxonil result in a TcsC-dependent phosphorylation of SakA, the final MAP kinase in the high osmolarity glycerol (HOG) pathway, confirming a role for TcsC in this signaling pathway.Several types of stress, such as hypoxia, exposure to farnesol or elevated concentrations of certain divalent cations, trigger a differentiation in A. fumigatus toward a "fluffy" growth phenotype resulting in white, dome-shaped colonies.Although TcsC plays a role in the adaptation of A. fumigatus to hypoxia, it seems to be dispensable for virulence.

View Article: PubMed Central - PubMed

Affiliation: Max-von-Pettenkofer-Institut, Ludwig-Maximilians-University, Munich, Germany.

ABSTRACT
Two-component signaling systems are widespread in bacteria, but also found in fungi. In this study, we have characterized TcsC, the only Group III two-component sensor kinase of Aspergillus fumigatus. TcsC is required for growth under hyperosmotic stress, but dispensable for normal growth, sporulation and conidial viability. A characteristic feature of the ΔtcsC mutant is its resistance to certain fungicides, like fludioxonil. Both hyperosmotic stress and treatment with fludioxonil result in a TcsC-dependent phosphorylation of SakA, the final MAP kinase in the high osmolarity glycerol (HOG) pathway, confirming a role for TcsC in this signaling pathway. In wild type cells fludioxonil induces a TcsC-dependent swelling and a complete, but reversible block of growth and cytokinesis. Several types of stress, such as hypoxia, exposure to farnesol or elevated concentrations of certain divalent cations, trigger a differentiation in A. fumigatus toward a "fluffy" growth phenotype resulting in white, dome-shaped colonies. The ΔtcsC mutant is clearly more susceptible to these morphogenetic changes suggesting that TcsC normally antagonizes this process. Although TcsC plays a role in the adaptation of A. fumigatus to hypoxia, it seems to be dispensable for virulence.

Show MeSH
Related in: MedlinePlus