Skip to main content

Advertisement

SpringerLink
Log in

Bioaerosol vertical fungal spores profile in Minas Gerais State, Brazil

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

Abstract

Primary biological aerosol particles (PBAPs) are involved in multiple phenomena ranging from seasonal allergies to pandemic diseases. Furthermore, PBAPs that act as ice nuclei, might interact with cloud physics affecting the formation of hail and, potentially, causing damage to agriculture. These latter dynamics are still unclear, especially due to the lack of knowledge about PBAPs concentration and emission rates. Here we characterized the fungal aerobiology of Arceburgo, Minas Gerais State, Brazil, through ground level and airborne sampling of PBAPs via a hot-air balloon. Total and cultivable fungal spores were collected using personal portable Burkard and a MAS100 sampler respectively during the summer and winter of 2019. In the latter season, daily dynamics were resolved by repeating flights and sampling in the morning and in the afternoon. Both samplers identified a core fungal community (Penicillum/Aspergillus and Cladosporium spp.) that are coupled with local meteorological dynamics and are able to undergo atmospheric transport as indicated by their survival in the night-time residual boundary layer. These results are invaluable in identifying a core set of aerobiological indicators that can be used in future works to unravel PBAPs emission rates on the area of Arceburgo and form a basis to close the gap in knowledge in the interplay between PBAPs and hail formation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Source: Google Earth)

Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Agrios, G. N. (2005). Plant diseases caused by fungi. Plant Pathology, 385–614.

  • Aizenberg, V., Reponen, T., Grinshpun, S. A., & Willeke, K. (2000). Performance of air-O-cell, Burkard, and button samplers for total enumeration of airborne spores. American Industrial Hygiene Association Journal, 61(6), 855–864.

    Article  CAS  Google Scholar 

  • Amador, G., Barberie, A., & Hu, D. (2021). Aerodynamics of puffball mushroom spore dispersal. APS, E17–004.

  • Ataygul, E., Celenk, S., Canitez, Y., et al. (2007). allergenic fungal spore concentrations in the atmosphere of Bursa, Turkey. Journal of Biological Environmental Science, 1(2), 73–79.

    Google Scholar 

  • Bensch, K., Braun, U., Groenewald, J. Z., & Crous, P. W. (2012). The genus cladosporium. Studies in Mycology, 72, 1–401.

    Article  CAS  Google Scholar 

  • Bezerra, G. F. B., et al. (2014). Diversity and dynamics of airborne fungi in São Luis, State of Maranhão, Brazil. Revista Da Sociedade Brasileira De Medicina Tropical, 47(1), 69–73.

    Article  Google Scholar 

  • Brickus, L. S., et al. (1998). Occurrence of airborne bacteria and fungi in bayside offices in Rio de Janeiro, Brazil. Indoor and Built Environment, 7(5–6), 270–275.

    Article  Google Scholar 

  • Bridge, P., & Spooner, B. (2001). Soil fungi: Diversity and detection. Plant and Soil, 232(1–2), 147–154.

    Article  CAS  Google Scholar 

  • Burch, M., & Levetin, E. (2002). Effects of meteorological conditions on spore plumes. International Journal of Biometeorology, 46(3), 107–117.

    Article  CAS  Google Scholar 

  • Carslaw, D. C., & Ropkins, K. (2021). openair: An R package for air quality data analysis. Environmental Modelling and Software, 27–28, 52–61.

    Google Scholar 

  • Castro E Silva, D. M., Santos, D. C. S., Pukinskas, S. R. B. S., et al. (2015). A new culture medium for recovering the agents of cryptococcosis from environmental sources. Brazilian Journal of Microbiology, 46(2), 355–358.

    Article  Google Scholar 

  • Crous, P. W., Braun, U., Schubert, K., & Groenewald, J. Z. (2007). Delimiting Cladosporium from morphologically similar genera. Studies in Mycology, 58, 33–56.

    Article  CAS  Google Scholar 

  • Degobbi, C. (2010). Análise dos contaminantes biológicos presentes no material particulado (PM2,5) de amostras da região metropolitana de São Paulo. 2010. 151 f. Tese (Doutorado em Ciência) - Programa de Pós-Graduação em Patologia. Faculdade de medicina da Universidade de São Paulo, São Paulo.

  • Degobbi, C., Lopes, F. D. T. Q. S., Carvalho-Oliveira, R., Muñoz, J. E., & Saldiva, P. H. N. (2011). Correlation of fungi and endotoxin with PM2.5 and meteorological parameters in atmosphere of Sao Paulo, Brazil. Atmospheric Environment, 45(13), 2277–2283.

    Article  CAS  Google Scholar 

  • Deleon-Rodriguez, N., Lathem, T. L., Rodriguez-R, L. M., Barazesh, J. M., Anderson, B. E., Beyersdorf, A. J., Ziemba, L. D., Bergin, M., Nenes, A., & Konstantinidis, K. T. (2013). Microbiome of the upper troposphere: Species composition and prevalence, effects of tropical storms, and atmospheric implications. Proceedings of the National Academy of Sciences of the United States of America, 110(7), 2575–2580. https://doi.org/10.1073/pnas.1212089110

    Article  Google Scholar 

  • Després, V. R., Alex Huffman, J., Burrows, S. M., et al. (2012). Primary biological aerosol particles in the atmosphere: A review. Tellus, Series B: Chemical and Physical Meteorology, 64 (1).

  • Dixon, P. A. (1961). Spore dispersal in Chaetomium globosum (Kunze). Nature, 191(4796), 1418–1419.

    Article  Google Scholar 

  • Douwes, J., Thorne, P., Pearce, N., & Heederik, D. (2003). Bioaerosol health effects and exposure assessment: Progress and prospects. Annals of Occupational Hygiene, 47(3), 187–200.

    CAS  Google Scholar 

  • de Hoog, G. S., Guarro, J., Gené, J., & Figueras, M. J. (2000). Atlas of clinical fungi (No. Ed. 2). Centraalbureau voor Schimmelcultures (CBS).

  • Elbert, W., Taylor, P. E., Andreae, M. O., & Pöschl, U. (2007). Contribution of fungi to primary biogenic aerosols in the atmosphere: Wet and dry discharged spores, carbohydrates, and inorganic ions. Atmospheric Chemistry and Physics, 7(17), 4569–4588.

    Article  CAS  Google Scholar 

  • Emygdio, A. P. M., Degobbi, C., Gonçalves, F. L. T., & Andrade, M. D. F. (2018). One year of temporal characterization of fungal spore concentration in São Paulo metropolitan area, Brazil. Journal of Aerosol Science, 115(121–132).

  • Feller, W. (1950). An introduction to the probability theory and its application (p. 175). New York: Wiley.

    Google Scholar 

  • Field, A.; Miles, J., & Field, Z. (2012). Discovering statistics using R. SAGE.

  • Fochesatto, G. J., Drobinski, P., Flamant, C., et al. (2001). Evidence of dynamical coupling between the residual layer and the developing convective boundary layer. Boundary-Layer Meteorology, 99, 451–464.

    Article  Google Scholar 

  • Fröhlich-Nowoisky, J., Kampf, C. J., Weber, B., et al. (2016). Bioaerosols in the Earth system: Climate, health, and ecosystem interactions. Atmospheric Research, 182, 346–376.

    Article  Google Scholar 

  • Giraudoux, P. (2018). pgirmess: Spatial analysis and data mining for field ecologists. R package version 1.6.9. https://CRAN.R-project.org/package=pgirmess

  • Griffin, D. W. (2004). Terrestrial microorganisms at an altitude of 20,000 m in Earth’s atmosphere. Aerobiologia, 20, 135–140.

    Article  Google Scholar 

  • Grinn-Gofroń, A., & Rapiejko, P. (2009). Occurrence of Cladosporium spp. and Alternaria spp. spores in Western, Northern and Central-Eastern Poland in 2004–2006 and relation to some meteorological factors. Atmospheric Research, 93(4), 747–758.

    Article  Google Scholar 

  • Grosjean, P., & Ibanez, F. (2018). pastecs: Package for analysis of space-time ecological series. R package version 1.3.21. https://CRAN.R-project.org/package=pastecs

  • Haines, J., Escamilla, B., Muilenberg, M. L., Gallup, J., & Levetin, E (2000). Mycology of the air. An introduction to the sampling and identification of airborne fungus spores. Tucson, Arizona.

  • Hawksworth, D. L. (1991). The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycological Research, 95(6), 641–655. British Mycological Society.

  • Hawksworth, D., & Gardens, R. B. (2017). Fungal diversity revisited: 2.2 to 3.8 Million Species. Microbiology Spectrum, 5(4), 79–95.

    Article  Google Scholar 

  • Hersbach, H., Bell, B., Berrisford, P., Biavati, G., Horányi, A., Muñoz Sabater, J., Nicolas, J., Peubey, C., Radu, R., Rozum, I., Schepers, D., Simmons, A., Soci, C., Dee, D., & Thépaut, J-N. (2018a). ERA5 hourly data on single levels from 1979 to present. Copernicus Climate Change Service (C3S) Climate Data Store (CDS).

  • Hersbach, H., Bell, B., Berrisford, P., Biavati, G., Horányi, A., Muñoz Sabater, J., Nicolas, J., Peubey, C., Radu, R., Rozum, I., Schepers, D., Simmons, A., Soci, C., Dee, D., & Thépaut, J.-N. (2018b). ERA5 hourly data on pressure levels from 1979 to present. Copernicus Climate Change Service (C3S) Climate Data Store (CDS).

  • Lucca, A. J. D. (2007). Harmful fungi in both agriculture and medicine. Revista Iberoamericana De Micologia, 24(1), 3–13.

    Article  Google Scholar 

  • Marple, V. A., & Olson, B. A. (2011). Sampling and measurement using inertial, gravitational, centrifugal, and thermal techniques. Aerosol Measurement: Principles, Techniques, and Applications: Third Edition, 129–151.

  • Martins, J. A., Brand, V. S., Capucim, M. N., et al. (2017). Climatology of destructive hailstorms in Brazil. Atmospheric Research, 184, 126–138.

    Article  Google Scholar 

  • Matthias-Maser, S., & Jaenicke, R. (1995). The size distribution of primary biological aerosol particles with radii > 0.2 [mu]m in an urban/rural influenced region. Atmospheric Research, 39(4), 279–286.

    Article  Google Scholar 

  • Meier, R., & Zingre, H. (2000). Qualification of air sampler systems: The MAS-100. Swiss Pharma, 22(1–2), 15–21.

    Google Scholar 

  • Morris, C. E., Conen, F., Alex Huffman, J., Phillips, V., Pöschl, U., & Sands, D. C. (2014). Bioprecipitation: A feedback cycle linking Earth history, ecosystem dynamics and land use through biological ice nucleators in the atmosphere. Global Change Biology, 20(2), 341–351. https://doi.org/10.1111/gcb.12447

    Article  Google Scholar 

  • Morris, C. E., Sands, D. C., Bardin, M., Jaenicke, R., Vogel, B., Leyronas, C., Ariya, P. A., & Psenner, R. (2008). Microbiology e atmospheric processes: An upcoming era of research on bio-meteorology. Biogeosciences Discussion, 5, 191–212.

    Google Scholar 

  • Morris, C. E., Sands, D. C., Bardin, M., Jaenicke, R., Vogel, B., Leyronas, C., Ariya, P. A., & Psenner, R. (2011). Microbiology e atmospheric processes: Research challenges concerning the impact of airborne micro-organisms on the atmosphere e climate. Biogeosciences, 8, 17–25.

    Article  CAS  Google Scholar 

  • Morris, C. E., Sands, D. C., Glaux, C., Samsatly, J., Asaad, S., Moukahel, A. R., Gonçalves, F. L. T., & Bigg, E. K. (2012). Urediospores of rust fungi are ice nucleation active at > −10ºC e harbor ice nucleation active bacteria. Atmospheric Chemistry e Physics, 13, 4223–4233.

    Article  Google Scholar 

  • Murray, B. J., O’sullivan, D., Atkinson, J. D., & Webb, M. E. (2012). Ice nucleation by particles immersed in supercooled cloud droplets. Chemical Society Reviews, 41(19), 6519.

    Article  CAS  Google Scholar 

  • Nagarajan, S., & Singh, D. V. (1990). Long-distance dispersion of rust pathogens. Annual Review of Phytopathology, 28(1), 139–153.

    Article  CAS  Google Scholar 

  • NASA/METI/AIST/Japan Spacesystems and U.S./Japan ASTER Science Team. ASTER Global Digital Elevation Model V003. NASA EOSDIS Land Processes DAAC, 2019.

  • Oke, T. R. (1987). Boundary layer climates, 2nd ed. Routledge (Taylor & Francis group).

  • Pace, L., Boccacci, L., Casilli, M., & Fattorini, S. (2019). Temporal variations in the diversity of airborne fungal spores in a Mediterranean high altitude site. Atmospheric Environment, 210, 166–170.

    Article  CAS  Google Scholar 

  • Pöschl, U., Martin, S. T., Sinha, B., et al. (2010). Rainforest aerosols as biogenic nuclei of clouds and precipitation in the Amazon. Science, 329(5998), 1513–1516.

    Article  Google Scholar 

  • R Core Team. R: A language and environment for statistical computing. (2020). R Foundation for Statistical Computing, Vienna, Austria.https://www.R-project.org/.

  • Reponen, T., Grinshpun, S. A., Conwell, K. L., Wiest, J., & Anderson, M. (2001). Aerodynamic versus physical size of spores: Measurement and implication for respiratory deposition. Grana, 40(3), 119–125.

    Article  Google Scholar 

  • Revelle, W. (2020). psych: Procedures for Personality and Psychological Research, Northwestern University, Evanston, Illinois, USA. https://CRAN.R-project.org/package=psych Version = 2.0.8.

  • Rogers, C., & Muilenberg, M. L. (2001). Comprehensive guidelines for the operation of hirst-type suction bioaerossol samplers. Pan-American Aerobiology Association, Standardized Protocols.

  • Rosenfeld, D., Lohmann, U., Raga, G. B., et al. (2008). Flood or drought: how do aerosols affect precipitation? Science (new York, NY), 321(5894), 1309–1313.

    Article  CAS  Google Scholar 

  • Seinfeld, J. H., Bretherton, C., Carslaw, K. S., et al. (2016). Improving our fundamental understanding of the role of aerosol−cloud interactions in the climate system. Proceedings of the National Academy of Sciences, 113(21), 5781–5790.

    Article  CAS  Google Scholar 

  • Shoemaker, R. A., & Babcock, C. E. (1989). Phaeosphaeria. Canadian Journal of Botany, 67(5), 1500–1599.

    Article  Google Scholar 

  • Smith, E. G. (1984). Sampling and identifying allergenic pollens and molds. Blewstone Press.

    Google Scholar 

  • Lighthart & Stetzenbach. (1994). Distribution of Microbial Bioaerosol. In: Lighthart, B. and Mohr, A. J. (Eds.) Atmospheric microbial aerosols. New York: Chapman & Hall.

  • Stull, R. B. (1988). An Introduction to Boundary Layer Meteorology (p. 666). Kluwer Academic Publishers.

    Book  Google Scholar 

  • Wainwright, M., Wickramasinghe, N. C., Narlikar, J. V., & Rajaratnam, P. (2003). Microorganisms cultured from stratospheric air samples obtained at 41 km. FEMS Microbiology Letters, 218(1), 161–165. https://doi.org/10.1016/S0378-1097(02)01138-2

    Article  CAS  Google Scholar 

  • Wang, X. W., Houbraken, J., Groenewald, J. Z., Meijer, M., Andersen, B., Nielsen, K. F., et al. (2016). Diversity and taxonomy of Chaetomium and chaetomium-like fungi from indoor environments. Studies in Mycology, 84, 145–224.

    Article  CAS  Google Scholar 

  • WFCC (World data center for microorganisms). (2020). Culture collection information worldwide. http://www.wfcc.info/ccinfo/statistics/

  • Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. Springer, New York. https://cran.r-project.org/web/packages/ggplot2/ggplot2.pdf

  • Wickham, H., & Bryan, J. (2019). readxl: Read Excel Files. R package version 1.3.1. https://CRAN.R-project.org/package=readxl

  • Wickham, H., François, R., Henry, L. & Müller, K. (2020). dplyr: A Grammar of Data Manipulation. R package version 1.0.2. https://CRAN.R-project.org/package=dplyr

  • Yao, M., & Mainelis, G. (2006). Investigation of cut-off sizes and collection efficiencies of portable microbial samplers. Aerosol Science and Technology, 40(8), 595–606.

    Article  CAS  Google Scholar 

  • Zhirnov, A. A., Kudryashova, N. N., Kudryashova, O. B., Korovina, N. V., Pavlenko, A. A., & Titov, S. S. (2019). Spores of puffball fungus Lycoperdon pyriforme as a reference standard of stable monodisperse aerosol for calibration of optical instruments. PLoSO, 14(1).

Download references

Acknowledgements

The authors are grateful to the balloonist Luiz Eduardo Consiglio and Jairo Antonio Dia Santos Fogaça and to the others crew members. Authors are especially glad to the collaborators and farm owners where the sampling took place. Special thanks to Prof. Dr. Pedro Leite da Silva Dias and Prof. Dr. Maria Assunção Faus da Silva Dias for their assistance with the sampling and data analyzes.

Funding

This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, São Paulo Research Foundation; Grants 2016/06160-8 and 2016/10594-3) and by the Brazilian Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Office for the Advancement of Higher Education).

Author information

Authors and Affiliations

  1. Institute of Astronomy, Geophysics and Atmospheric Science (IAG), University of São Paulo (USP), R. do Matão, 1226 - Butantã, São Paulo, SP, 05508-090, Brazil

    Ana Paula Mendes Emygdio, Cristiane Degobbi, Thaysla Beluco Quintino, Rafael Henrique de Souza Zanetti, Mauricio C. Mantoani, Pedro Leite da Silva Dias & Fábio Luiz Teixeira Gonçalves

  2. Institute of BioEconomy (IBE), National Research Council of Italy (CNR), Florence, Italy

    Federico Carotenuto

  3. Department of Micology, Adolfo Lutz Institute, Sao Paulo, Brazil

    Dulcilena de Matos Castro e Silva

  4. Laboratory of Research in Marine Environmental Monitoring (LAPMAR), Geosciences Institute, Federal University of Pará, Belém, Brazil

    Solana Meneghel Boschilia

  5. Interunities Graduate Program in Biotechnology, University of São Paulo, Sao Paulo, Brazil

    Lara Chaves Carvalho Guerra

  6. Unité de Pathologie Végétale UR407, INRAE, Montfavet, France

    Cindy E. Morris

Authors
  1. Ana Paula Mendes Emygdio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristiane Degobbi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Federico Carotenuto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dulcilena de Matos Castro e Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thaysla Beluco Quintino
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rafael Henrique de Souza Zanetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mauricio C. Mantoani
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Solana Meneghel Boschilia
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lara Chaves Carvalho Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Pedro Leite da Silva Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Cindy E. Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Fábio Luiz Teixeira Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

APME and FLTG designed the research project; APME, CD, DMCS, TBQ, RHSZ, SMB performed the data collection and analyzes; APME, CD, FC, DMCS, TBQ, RHSZ, MCM, SMB, LCCG, PLSD, CEM, FLTG wrote and edited the manuscript; APME and FLTG led the manuscript writing; all authors contributed to all versions and gave approval to the final version of the manuscript.

Corresponding author

Correspondence to Ana Paula Mendes Emygdio.

Ethics declarations

Conflict interest

The author declare that they have no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Emygdio, A.P.M., Degobbi, C., Carotenuto, F. et al. Bioaerosol vertical fungal spores profile in Minas Gerais State, Brazil. Aerobiologia 38, 85–101 (2022). https://doi.org/10.1007/s10453-021-09736-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10453-021-09736-1

Keywords

Search

Navigation