Elastin increases biofilm and extracellular matrix production of <i>Aspergillus fumigatus</i>

Aspergillus fumigatus is an opportunistic saprobe fungus that accounts for 90% of cases of pulmonary aspergillosis in immunosuppressed patients and is known for its angiotropism. When it reaches the respiratory tract, A. fumigatus interacts with structural components and blood vessels of the lungs, such as elastin. To understand the effect of this structural component, we examined the effect of elastin on the production and development of the biofilm of A. fumigatus. In RPMI containing 10 mg/mL of elastin, a significant increase (absorbance p < 0.0001; dry weight p < 0.0001) in the production of biofilm was observed in comparison to when RPMI was used alone, reaching a maximum growth of 18.8 mg (dry weight) of biofilm in 72 h. In addition, elastin stimulates the production (p = 0.0042) of extracellular matrix (ECM) and decreases (p = 0.005) the hydrophobicity during the development of the biofilm. These results suggest that elastin plays an important role in the growth of A. fumigatus and that it participates in the formation of thick biofilm.

Keywords:
Aspergillus fumigatus; Biofilm; Elastin; Extracellular matrix; Hydrophobicity

Authorship

Ildnay de Souza Lima Brandão

Universidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Micologia, Cidade Universitária, PE, BrazilUniversidade Federal de PernambucoBrazilCidade Universitária, PE, BrazilUniversidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Micologia, Cidade Universitária, PE, Brazil

Heloiza Maria da Silva Oliveira-Moraes

Universidade Federal de Pernambuco, Centro de Ciências Biológicas Rua Departamento de Micologia, Cidade Universitária, PE, BrazilUniversidade Federal de PernambucoBrazilCidade Universitária, PE, BrazilUniversidade Federal de Pernambuco, Centro de Ciências Biológicas Rua Departamento de Micologia, Cidade Universitária, PE, Brazil

Cristina Maria de Souza Motta

Universidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Micologia, Pernambuco, PE, BrazilUniversidade Federal de PernambucoBrazilPernambuco, PE, BrazilUniversidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Micologia, Pernambuco, PE, Brazil

Neiva Tinti de Oliveira

Oliane Maria Correia Magalhães ^**Corresponding author. E-mail: olimicomed@yahoo.com.br (O.M. Magalhães).

*Corresponding author. E-mail: olimicomed@yahoo.com.br (O.M. Magalhães).

Conflicts of interest

The authors declare that they have no competing interests.

Associate Editor: Waldir Elias

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Figures

Figures (5)

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Fig. 1
Influence of elastin on the growth of A. fumigatus biofilm. The graphics represent the mean values with SDs of the biofilm production of both isolates of A. fumigatus measured by absorbance with 0.5% crystal violet (A) and (B) the dry weight. A significant increase in the presence of 10 mg/mL of elastin (gray bars) compared to RPMI alone (black bars) was observed for all time periods (**p < 0.01; ****p < 0.0001; ANOVA); (C) A. fumigatus URM6575 biofilm grown in RPMI is shown after 48 h at 37 °C under light in microscopy and (D) stained with Calcofluor White^® (E) and in RPMI supplemented with 10 mg/mL of elastin under microscopy and (F) stained with Calcofluor White^®. An increased amount of biofilm was produced in the presence of elastin (10 mg/mL). Circular arrangements (yellow arrow) and parallel bundles of hyphae (black arrow) are shown. Scale bar, 50 µm.

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Fig. 2
Influence of elastin on extracellular matrix (ECM) of A. fumigatus biofilm. The means and SDs show that the amount of ECM produced in the presence of elastin (gray bars) was significantly greater (p = 0.0042), than that produced in RPMI alone (black bars). The difference between isolates of clinical (URM6573) and environmental (URM5992) origin was highly significant (p < 0.001, ANOVA). **p < 0.01; ****p < 0.0001.

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Fig. 3
Enhanced production extracellular matrix (ECM) of A. fumigatus biofilm. Photomicrographs taken by scanning electron microscopy analysis of A. fumigatus URM6575 biofilm in RPMI (A) and RPMI with elastin (B) show increased production of ECM in the presence of elastin (yellow arrow). Magnification of 2000×. A. fumigatus URM6575 biofilm grown in RPMI supplemented with 10 mg/mL of elastin (C) under light microscopy and stained with concanavalin A-Alexa Fluor 488^® (D) show greater amounts of ECM at the ends of the hyphae (white arrow). Scale bar, 50 µm.

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Fig. 4
Influence of elastin on the hydrophobicity of A. fumigatus biofilm. The hydrophobicity in the presence of elastin (gray bars) was significantly lower (p = 0.005) than that in RPMI alone (black bars). The difference between the clinical (URM6573) and environmental (URM5992) isolates was highly significant (p < 0.0001, ANOVA). **p < 0.01; ****p < 0.0001.

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Fig. 5
Decreased hydrophobicity of A. fumigatus biofilm. A. fumigatus URM5992 (environmental origin) biofilm after 48 h at 37 °C. (A and B) Biofilm Grown in RPMI without elastin under light microscopy and stained with latex beads, respectively. (C and D) biofilm grown in RPMI with elastin - 10 mg/mL under light microscopy and stained with latex beads, respectively. Scale bar, 50 µm.

Fig. 1 Influence of elastin on the growth of A. fumigatus biofilm. The graphics represent the mean values with SDs of the biofilm production of both isolates of A. fumigatus measured by absorbance with 0.5% crystal violet (A) and (B) the dry weight. A significant increase in the presence of 10 mg/mL of elastin (gray bars) compared to RPMI alone (black bars) was observed for all time periods (p < 0.01; **p < 0.0001; ANOVA); (C) A. fumigatus URM6575 biofilm grown in RPMI is shown after 48 h at 37 °C under light in microscopy and (D) stained with Calcofluor White^® (E) and in RPMI supplemented with 10 mg/mL of elastin under microscopy and (F) stained with Calcofluor White^®. An increased amount of biofilm was produced in the presence of elastin (10 mg/mL). Circular arrangements (yellow arrow) and parallel bundles of hyphae (black arrow) are shown. Scale bar, 50 µm.

Fig. 2 Influence of elastin on extracellular matrix (ECM) of A. fumigatus biofilm. The means and SDs show that the amount of ECM produced in the presence of elastin (gray bars) was significantly greater (p = 0.0042), than that produced in RPMI alone (black bars). The difference between isolates of clinical (URM6573) and environmental (URM5992) origin was highly significant (p < 0.001, ANOVA). p < 0.01; **p < 0.0001.

Fig. 3 Enhanced production extracellular matrix (ECM) of A. fumigatus biofilm. Photomicrographs taken by scanning electron microscopy analysis of A. fumigatus URM6575 biofilm in RPMI (A) and RPMI with elastin (B) show increased production of ECM in the presence of elastin (yellow arrow). Magnification of 2000×. A. fumigatus URM6575 biofilm grown in RPMI supplemented with 10 mg/mL of elastin (C) under light microscopy and stained with concanavalin A-Alexa Fluor 488^® (D) show greater amounts of ECM at the ends of the hyphae (white arrow). Scale bar, 50 µm.

Fig. 4 Influence of elastin on the hydrophobicity of A. fumigatus biofilm. The hydrophobicity in the presence of elastin (gray bars) was significantly lower (p = 0.005) than that in RPMI alone (black bars). The difference between the clinical (URM6573) and environmental (URM5992) isolates was highly significant (p < 0.0001, ANOVA). p < 0.01; **p < 0.0001.

Fig. 5 Decreased hydrophobicity of A. fumigatus biofilm. A. fumigatus URM5992 (environmental origin) biofilm after 48 h at 37 °C. (A and B) Biofilm Grown in RPMI without elastin under light microscopy and stained with latex beads, respectively. (C and D) biofilm grown in RPMI with elastin - 10 mg/mL under light microscopy and stained with latex beads, respectively. Scale bar, 50 µm.

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Sociedade Brasileira de Microbiologia USP - ICB III - Dep. de Microbiologia, Sociedade Brasileira de Microbiologia, Av. Prof. Lineu Prestes, 2415, Cidade Universitária, 05508-900 São Paulo, SP - Brasil, Ramal USP 7979, Tel. / Fax: (55 11) 3813-9647 ou 3037-7095 - São Paulo - SP - Brazil
E-mail: bjm@sbmicrobiologia.org.br

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Elastin increases biofilm and extracellular matrix production of <i>Aspergillus fumigatus</i>

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[1] *Corresponding author. E-mail: olimicomed@yahoo.com.br (O.M. Magalhães).