Skip to main content

Advertisement

Log in

Germination dynamics of allergenic fungal spores in respiratory mucus

  • Original Paper
  • Published:
Aerobiologia Aims and scope Submit manuscript

Abstract

Mucus and body temperature serve as the first lines of defense against invading pathogens. When the inhaled particles are deposited in the nose, the respiratory mucus and body temperature potentially impact fungal spore germination and prevent pathogen infections. We hypothesized that respiratory mucus and body temperature impact fungal spore germination. This study aimed to investigate the temporal germination dynamics of allergenic Cladosporium, Aspergillus, and Penicillium spp. in respiratory mucus ex situ and the effect of the temperature (28 °C and 37 °C in the upper and lower respiratory tract, respectively) on fungal germination. Fungal spore germination was inhibited at 37 °C in C. oxysporum and C. cladosporioides, but not A. flavus, A. brunneoviolaceus, A. protuberus, P. citrinum, and P. oxalicum. Aspergillus flavus and A. brunneoviolaceus exhibited a high germination rate in the mucus at 28 °C and 37 °C. This indicated that their germination was not limited in the mucus in the upper or lower respiratory tract, where spores of these fungi can overcome the inhibition of germination as in invasive aspergillosis pathogens. The germination rate of A. protuberus in the mucus was very low at both 28 °C and 37 °C. Spore germination of P. citrinum and P. oxalicum occurred at 37 °C (normal body temperature) but was inhibited by the mucus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Achatz, G., Oberkofler, H., Lechenauer, E., Simon, B., Unger, A., Kandler, D., et al. (1995). Molecular cloning of major and minor allergens of Alternaria alternata and Cladosporium herbarum. Molecular Immunology, 32, 213–227.

    Article  CAS  Google Scholar 

  • Agarwal, R., & Gupta, D. (2011). Severe asthma and fungi: Current evidence. Medical Mycology, 49, S150–S157.

    Article  Google Scholar 

  • Bains, S. N., & Judson, M. A. (2012). Allergic bronchopulmonary aspergillosis. Clinics in Chest Medicine, 33, 265–281.

    Article  Google Scholar 

  • Borsa, B. A., Özgün, G., Houbraken, J., & Ökmen, F. (2015). The first case of persistent vaginitis due to Aspergillus protuberus in an immunocompetent patient. Mikrobiyoloji Bulteni, 49, 130–134.

    Article  Google Scholar 

  • Chen, B.-Y., Jasmine Chao, H., Wu, C.-F., Kim, H., Honda, Y., & Guo, Y. L. (2014). High ambient Cladosporium spores were associated with reduced lung function in schoolchildren in a longitudinal study. The Science of the Total Environment, 481, 370–376.

    Article  CAS  Google Scholar 

  • Cole, A. M., Dewan, P., & Ganz, T. (1999). Innate antimicrobial activity of nasal secretions. Infection and Immunity, 67, 3267–3275.

    Article  CAS  Google Scholar 

  • Dreborg, S. (1989). The skin prick test in the diagnosis of atopic allergy. Journal of the American Academy of Dermatology, 21, 820–821.

    Article  CAS  Google Scholar 

  • Fleming, A. (1922). On a remarkable bacteriolytic element found in tissues and secretions. Proceedings of the Royal Society of London. Series B, Containing Papers of a Biological Character, 93, 306–317.

    Article  CAS  Google Scholar 

  • Green, B. J., Mitakakis, T. Z., & Tovey, E. R. (2003). Allergen detection from 11 fungal species before and after germination. Journal of Allergy and Clinical Immunology, 111, 285–289.

    Article  Google Scholar 

  • Green, B. J., Tovey, E. R., Beezhold, D. H., Perzanowski, M. S., Acosta, L. M., Divjan, A. I., et al. (2009). Surveillance of fungal allergic sensitization using the fluorescent halogen immunoassay. Journal de Mycologie Medicale, 19, 253–261.

    Article  Google Scholar 

  • Hedayati, M. T., Pasqualotto, A. C., Warn, P. A., Bowyer, P., & Denning, D. W. (2007). Aspergillus flavus: Human pathogen, allergen and mycotoxin producer. Microbiology, 153, 1677–1692.

    Article  CAS  Google Scholar 

  • Horner, W. E., Helbling, A., Salvaggio, J. E., & Lehrer, S. B. (1995). Fungal allergens. Clinical Microbiology Reviews, 8, 161–179.

    Article  CAS  Google Scholar 

  • Hsu, N.-Y., Chen, P.-Y., Chang, H.-W., & Su, H.-J. (2011). Changes in profiles of airborne fungi in flooded homes in southern Taiwan after Typhoon Morakot. Science of the Total Environment, 409, 1677–1682.

    Article  CAS  Google Scholar 

  • Janahi, I. A., Rehman, A., & Al-Naimi, A. R. (2017). Allergic bronchopulmonary aspergillosis in patients with cystic fibrosis. Annals of Thoracic Medicine, 12, 74–82.

    Article  CAS  Google Scholar 

  • Jia, J., Chen, M., Mo, X., Liu, J., Yan, F., Li, Z., et al. (2019). The first case report of kerion-type scalp mycosis caused by Aspergillus protuberus. BMC Infectious Diseases, 19, 506.

    Article  Google Scholar 

  • Jurjevic, Z., Peterson, S. W., & Horn, B. W. (2012). Aspergillus section Versicolores: nine new species and multilocus DNA sequence based phylogeny. IMA fungus, 3, 59–79.

    Article  Google Scholar 

  • Kaliner, M. A. (1991). Human nasal respiratory secretions and host defense. American Review of Respiratory Disease, 144, S52–S56.

    Article  CAS  Google Scholar 

  • Kaliner, M. A. (1992). Human nasal host defense and sinusitis. Journal of Allergy and Clinical Immunology, 90, 424–430.

    Article  CAS  Google Scholar 

  • Kamei, K., & Watanabe, A. (2005). Aspergillus mycotoxins and their effect on the host. Medical Mycology, 1, S95–S99.

    Article  Google Scholar 

  • Kozak, P. P., Jr., Gallup, J., Cummins, L. H., & Gillman, S. A. (1980). Currently available methods for home mold surveys. II. Examples of problem homes surveyed. Annals of Allergy, 45, 167–176.

    Google Scholar 

  • Kurup, V. P., Shen, H.-D., & Banerjee, B. (2000). Respiratory fungal allergy. Microbes and Infection, 2, 1101–1110.

    Article  CAS  Google Scholar 

  • Lackner, A., Stammberger, H., Buzina, W., Freudenschuss, K., Panzitt, T., Schosteritsch, S., et al. (2005). Fungi: A normal content of human nasal mucus. American Journal of Rhinology, 19, 125–129.

    Article  Google Scholar 

  • Lee, R. J., Workman, A. D., Carey, R. M., Chen, B., Rosen, P. L., Doghramji, L., et al. (2016). Fungal aflatoxins reduce respiratory mucosal ciliary function. Scientific Reports, 6, 33221.

    Article  CAS  Google Scholar 

  • Levitz, S. M., & Diamond, R. D. (1985). Mechanisms of resistance of Aspergillus fumigatus conidia to killing by neutrophils in vitro. Journal of Infectious Diseases, 152, 33–42.

    Article  CAS  Google Scholar 

  • Lin, W.-R., Wang, P.-H., Tien, C.-J., Chen, W.-Y., Yu, Y.-A., & Hsu, L.-Y. (2018). Changes in airborne fungal flora along an urban to rural gradient. Journal of Aerosol Science, 116, 116–123.

    Article  CAS  Google Scholar 

  • Ma, J., Dong, J., Shang, Y., Inthavong, K., Tu, J., & Frank-Ito, D. O. (2018). Air conditioning analysis among human nasal passages with anterior anatomical variations. Medical Engineering & Physics, 57, 19–28.

    Article  Google Scholar 

  • Mitakakis, T. Z., Barnes, C., & Tovey, E. R. (2001). Spore germination increases allergen release from Alternaria. Journal of Allergy and Clinical Immunology, 107, 388–390.

    Article  CAS  Google Scholar 

  • Mitchell, C. G., Slight, J., & Donaldson, K. (1997). Diffusible component from the spore surface of the fungus Aspergillus fumigatus which inhibits the macrophage oxidative burst is distinct from gliotoxin and other hyphal toxins. Thorax, 52, 796–801.

    Article  CAS  Google Scholar 

  • Paulussen, C., Hallsworth, J. E., Álvarez-Pérez, S., Nierman, W. C., Hamill, P. G., Blain, D., et al. (2017). Ecology of aspergillosis: Insights into the pathogenic potency of Aspergillus fumigatus and some other Aspergillus species. Microbial Biotechnology, 10, 296–322.

    Article  Google Scholar 

  • Perfect, J. R. (2012). The impact of the host on fungal infections. The American Journal of Medicine, 125, S39–S51.

    Article  CAS  Google Scholar 

  • Perrone, G., Stea, G., Kulathunga, C. N., Wijedasa, H., & Arseculeratne, S. N. (2013). Aspergillus fijiensis sp. isolated from bronchial washings in a human case of bronchiectasis with invasive aspergillosis: The first report. Microbiology Discovery, 1, 9.

    Article  Google Scholar 

  • Pfavayi, L. T., Sibanda, E. N., & Mutapi, F. (2020). The pathogenesis of fungal-related diseases and allergies in the African population: The state of the evidence and knowledge gaps. International Archives of Allergy and Immunology, 181, 257–269.

    Article  Google Scholar 

  • Philippe, B., Ibrahim-Granet, O., Prevost, M. C., Gougerot-Pocidalo, M. A., Perez, M. S., Van der Meeren, A., et al. (2003). Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infection and Immunity, 71, 3034–3042.

    Article  CAS  Google Scholar 

  • Pynnonen, M., Stephenson, R. E., Schwartz, K., Hernandez, M., & Boles, B. R. (2011). Hemoglobin promotes Staphylococcus aureus nasal colonization. PLoS Pathogens, 7, e1002104.

    Article  CAS  Google Scholar 

  • R Core Team. (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

  • Reponen, T. (1995). Aerodynamic diameters and respiratory deposition estimates of viable fungal particles in mold problem dwellings. Aerosol Science and Technology, 22, 11–23.

    Article  Google Scholar 

  • Rocchi, S., Reboux, G., Larosa, F., Scherer, E., Daguindeau, E., Berceanu, A., et al. (2014). Evaluation of invasive aspergillosis risk of immunocompromised patients alternatively hospitalized in hematology intensive care unit and at home. Indoor Air, 24, 652–661.

    Article  CAS  Google Scholar 

  • Sephton-Clark, P. C., & Voelz, K. (2018). Spore germination of pathogenic filamentous fungi. In S. Sariaslani & G. M. Gadd (Eds.), Advances in applied microbiology (pp. 117–157). Cambridge: Academic Press.

    Google Scholar 

  • Sercombe, J. K., Green, B. J., & Tovey, E. R. (2006). Recovery of germinating fungal conidia from the nasal cavity after environmental exposure. Aerobiologia, 22, 295–304.

    Article  Google Scholar 

  • Shih, F. M., Lin, W. R., Wang, P. H., Lee, M. F., & Chen, Y. H. (2017). Airborne-allergenic fungal spora and seroepidemiology in Taiwan. In Proceedings of the microbiological society of Korea conference, April 25–April 30, 2017. Busan, Korea (pp. 158–158).

  • Tanaka, R. J., Boon, N. J., Vrcelj, K., Nguyen, A., Vinci, C., Armstrong-James, D., et al. (2015). In silico modeling of spore inhalation reveals fungal persistence following low dose exposure. Scientific Reports, 5, 13958.

    Article  CAS  Google Scholar 

  • Tomee, J. F., & Kauffman, H. F. (2000). Putative virulence factors of Aspergillus fumigatus. Clinical and Experimental Allergy: Journal of the British Society for Allergy and Clinical Immunology, 30, 476–484.

    Article  CAS  Google Scholar 

  • Wei, D.-L., Chen, J.-H., Jong, S.-C., & Shen, H.-D. (1993). Indoor airborne Penicillium species in Taiwan. Current Microbiology, 26, 137–140.

    Article  Google Scholar 

  • Woo, A. C., Brar, M. S., Chan, Y., Lau, M. C. Y., Leung, F. C. C., Scott, J. A., et al. (2013). Temporal variation in airborne microbial populations and microbially-derived allergens in a tropical urban landscape. Atmospheric Environment, 74, 291–300.

    Article  CAS  Google Scholar 

  • Wu, P.-C., Tsai, J.-C., Li, F.-C., Lung, S.-C., & Su, H.-J. (2004). Increased levels of ambient fungal spores in Taiwan are associated with dust events from China. Atmospheric Environment, 38, 4879–4886.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The study was funded by the Environmental Analysis Laboratory, Environmental Protection Administration, Executive Yuan, Taiwan (EPA-102-E3S5-02-02) and Taichung Veterans General Hospital, Taiwan (TCVGH-T1047807) to P. H Wang.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pi-Han Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, WR., Chen, SY., Hsiao, SC. et al. Germination dynamics of allergenic fungal spores in respiratory mucus. Aerobiologia 37, 271–279 (2021). https://doi.org/10.1007/s10453-020-09689-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10453-020-09689-x

Keywords

Navigation