Abstract
Bioaerosols are particles of great importance for several fields of research, and spores produced by fungi can exist as bioaerosols when suspended in the air. Microbiological standards for environmental monitoring of outdoor air parameters can be achieved by analyzing the relationship between airborne microorganisms and the prevailing environmental conditions. The outdoor air of the Metropolitan Region of São Paulo and the rural area in a city of the state of São Paulo (Ibiúna/SP), both in Brazil, were evaluated for the presence of microorganisms using the MAS-100 ECO (Merck®, Fr.) and M Air T (Millipore®) air sample collectors. Dichloran Rose-Bengal Chloramphenicol and Tryptic Soy Agars were used for fungal and bacterial isolation, respectively. Bacterial colonies were counted, and the plates with fungal colonies were sent for phenotypic identification up to genus and species level, respectively. Data on pollutant concentrations were obtained from the Environmental Company of the State of São Paulo. The highest number of Colony-Forming Units/m3 (CFU/m3) of microorganisms was measured in the winter and summer seasons, respectively, but the greatest Spore-Forming Units (SFU) of fungi were found in the rural area, where pollutant concentrations were lower. Nitrogen dioxide (NO2) had a slightly positive influence on the concentration of SFU of fungi in both areas studied. Sulfur dioxide (SO2) pollutant concentrations had both positive and negative great relations showing influence on microbial counts in the air of the rural area. In the rural area, the low bacteria count was influenced negatively by the low concentration of carbon monoxide (CO). The microbial counts were related to each other, as well as to the concentrations of pollutants, shown by all the correlations seen, indicating microorganisms as biomarkers of pollution in outdoor areas. The influence of environmental factors on the population and outdoor air biome is also explicit.
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References
BI17: Opportunistic fungal infection with Alternaria in the immunosuppressed. (2021). British Journal of Dermatology. Oxford Academic, 185(S1), pp. 150–150. https://doi.org/10.1111/bjd.20315
‘Resolução CONAMA No 491 DE 19_11_2018 - Federal - LegisWeb’ (no date).
Abdel Hameed, A. A., et al. (2012). Study on some factors affecting survivability of airborne fungi. Science of the Total Environment., 414, 696–700. https://doi.org/10.1016/j.scitotenv.2011.10.042
Aguiar, L. (2015). Estudo da relação da qualidade do ar e variáveis meteorológicas na ocorrência de morbidade respiratória e circulatória na Região Metropolitana de São Paulo, p. 105. Available at: http://repositorio.utfpr.edu.br/jspui/bitstream/1/1384/1/LD_PPGEA_M_Aguiar%2C Lais Sinhorini_2015.pdf (Accessed: 7 May 2018)
Amend, A. S., et al. (2010). Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proceedings of the National Academy of Sciences, 107(31), 13748–13753. https://doi.org/10.1073/pnas.1000454107
Andreeva, I. S., et al. (2024). Culturable microorganisms of aerosols sampled during aircraft sounding of the atmosphere over the Russian Arctic Seas. Atmosphere, 15, 365. https://doi.org/10.3390/ATMOS15030365
Arbex, M. A., et al. (2012). A poluição do ar e o sistema respiratório. Jornal Brasileiro De Pneumologia, 38(5), 643–655.
Bernardi, E. (2007). Fungos anemófilos e suas relações com fatores abióticos, na praia do Laranjal, Pelotas, RS. Revista De Biologia e Ciências Da Terra, 7(2), 91–96.
Borges, K. R. A., Monteiro, S. G., & Monteiro, C. A. (2012). Diversity and prevalence of airborne fungi isolated from São Luís, Northeast Brazil. Revista Brasileira De Análises Clínicas, 44(3–4), 132–138.
Brągoszewska, E., & Pastuszka, J. S. (2018). ‘Influence of meteorological factors on the level and characteristics of culturable bacteria in the air in Gliwice, Upper Silesia (Poland). Aerobiologia, 34(2), 241–255. https://doi.org/10.1007/s10453-018-9510-1
Burrows, S. M., et al. (2009). Bacteria in the global atmosphere – Part 2: Modelling of emissions and transport between different ecosystems. Atmospheric Chemistry and Physics Discussions, 9(3), 10829–10881. https://doi.org/10.5194/acpd-9-10829-2009
Carvalho, V. S. B., et al. (2015). Air quality status and trends over the Metropolitan Area of São Paulo, Brazil as a result of emission control policies. Environmental Science & Policy, 47(November), 68–79. https://doi.org/10.1016/j.envsci.2014.11.001
Chiquetto, J. B., et al. (2021). Impact of a truck Driver’s strike on air pollution levels in São Paulo. Atmospheric Environment, 246, 118072. https://doi.org/10.1016/j.atmosenv.2020.118072
Cuervo-Maldonado, S. I., et al. (2010). Actualización en Aspergilosis con énfasis en Aspergilosis invasora. Infectio, 14, 131–144.
Dannemiller, K. C., et al. (2016). Indoor microbial communities: Influence on asthma severity in atopic and nonatopic children. Journal of Allergy and Clinical Immunology. https://doi.org/10.1016/j.jaci.2015.11.027
de Matos Castro e Silva, D., et al. (2015). A new culture medium for recovering the agents of cryptococcosis from environmental sources. Brazilian Journal of Microbiology, 46(2), 355–358. https://doi.org/10.1590/S1517-838246220130726
Dong, L., et al. (2016). Concentration and size distribution of total airborne microbes in hazy and foggy weather. Science of the Total Environment, 541, 1011–1018. https://doi.org/10.1016/j.scitotenv.2015.10.001
Egan, C., Li, D. W., & Klironomos, J. (2014). Detection of arbuscular mycorrhizal fungal spores in the air across different biomes and ecoregions. Fungal Ecology, 12, 26–31. https://doi.org/10.1016/j.funeco.2014.06.004
El-Batrawy, O. A. (2010). Relationships between personal, indoor and outdoor PM 10 in the residential environment in Damietta, Egypt. Journal of American Science., 6, 1413.
Elbert, W., et al. (2006). Contribution of fungi to primary biogenic aerosols in the atmosphere: Active discharge of spores, carbohydrates, and inorganic ions by Asco- and Basidiomycota. Atmospheric Chemistry and Physics Discussions, 6, 11317–11355. https://doi.org/10.5194/acpd-6-11317-2006
Emygdio, A. P. M., Degobbib, C., Gonçalves, F. L. T., & de Fátima, A. M. (2018). ‘One year of temporal characterization of fungal spore concentration in São Paulo metropolitan Area Brazil. Journal of Aerosol Science, 115, 121–132.
Fan, X. Y., et al. (2019). More obvious air pollution impacts on variations in bacteria than fungi and their co-occurrences with ammonia-oxidizing microorganisms in PM2.5. Environmental Pollution. Elsevier Ltd, 251, 668–680. https://doi.org/10.1016/j.envpol.2019.05.004
Farmer, D. K., & Riches, M. (2020). Measuring biosphere-atmosphere exchange of short-lived climate forcers and their precursors. Accounts of Chemical Research, 53(8), 1427–1435. https://doi.org/10.1021/ACS.ACCOUNTS.0C00203
Filali Ben Sidel, F., et al. (2015). Airborne fungal spores of Alternaria, meteorological parameters and predicting variables. International Journal of Biometeorology, 59(3), 339–346. https://doi.org/10.1007/s00484-014-0845-1
Franić, I., et al. (2023). Climate, host and geography shape insect and fungal communities of trees. Scientific Reports. https://doi.org/10.1038/s41598-023-36795-w
Gao, M., et al. (2016). Variation of correlations between factors and culturable airborne bacteria and fungi. Atmospheric Environment, 128, 10–19. https://doi.org/10.1016/J.ATMOSENV.2015.12.008
Grinn-Gofroń, A., Strzelczak, A., & Wolski, T. (2011). The relationships between air pollutants, meteorological parameters and concentration of airborne fungal spores. Environmental Pollution, 159(2), 602–608. https://doi.org/10.1016/j.envpol.2010.10.002
Gutarowska, B., & Piotrowska, M. (2007). Methods of mycological analysis in buildings. Building and Environment, 42(4), 1843–1850. https://doi.org/10.1016/j.buildenv.2006.02.015
Heald, C. L., & Spracklen, D. V. (2009). Atmospheric budget of primary biological aerosol particles from fungal spores. Geophysical Research Letters. https://doi.org/10.1029/2009GL037493
Hoog, G. S., Guarro, J., Gené, G., & Figueras, M. (2014). Atlas of Clinical Fungi (3rd ed.). CBS-KNAW Fungal Biodiversity Centre.
Jasinski, R., Pereira, L. A. A., & Braga, A. L. F. (2011). Poluição atmosférica e internações hospitalares por doenças respiratórias em crianças e adolescentes em Cubatão, São Paulo, Brasil, entre 1997 e 2004. Cadernos De Saúde Pública, 27(11), 2242–2252. https://doi.org/10.1590/S0102-311X2011001100017
Jones, A. M., et al. (2004). The effects of meteorological factors on atmospheric bioaerosol concentrations - A review. Science of the Total Environment, 326(1–3), 151–180. https://doi.org/10.1016/j.scitotenv.2003.11.021
Lacey, J., & Venette, J. (2020). Outdoor Air Sampling Techniques, Bioaerosols Handbook. CRC Press, pp. 407–471. https://doi.org/10.1201/9781003070023-16.
Liu, H., et al. (2019). ‘The distribution variance of airborne microorganisms in urban and rural environments. Environmental Pollution, 247, 898–906. https://doi.org/10.1016/j.envpol.2019.01.090
Martins, L. C., et al. (2002). Poluição atmosférica e atendimentos por pneumonia e gripe em São Paulo Brasil. Revista De Saúde Pública, 36, 88–94. https://doi.org/10.1590/S0034-89102002000100014
Martins, M. S. D. A., Isabel, M., & Lemos, A. (2008). Liquens como bioindicadores da qualidade do ar numa área de termoelétrica, Rio Grande do Sul, Brasil. Hoehnea, 35(3), 425–433.
Mitchell, C. S., et al. (2007). Current state of the science: health effects and indoor environmental quality. Environmental Health Perspectives, 115(6), 958–964. https://doi.org/10.1289/ehp.8987
Morales-Oyervides, L., et al. (2020). Biotechnological approaches for the production of natural colorants by talaromyces/penicillium: a review. Biotechnology Advances. https://doi.org/10.1016/J.BIOTECHADV.2020.107601
Morris, C. E., Georgakopoulos, D. G., & Sands, D. C. (2004). Ice nucleation active bacteria and their potential role in precipitation. Journal De Physique IV, 121, 87–103. https://doi.org/10.1051/jp4:2004121004
Moura, M. L., Caldas, C. C., et al. (2015). The impaction capacity of Millipore M air T ® and Merck MAS- 100 ® in an external environment. Access Journal of Environmental Research, 1(November), 1–6.
Munzi, S., Ravera, S., & Caneva, G. (2007). Epiphytic lichens as indicators of environmental quality in Rome. Environmental Pollution, 146(2), 350–358. https://doi.org/10.1016/j.envpol.2006.03.042
Nowakowicz-Dębek, B., et al. (2017). Evaluating bioaerosol exposure among bus drivers in the public transport sector. Journal of Occupational and Environmental Hygiene, 14(11), D169–D172. https://doi.org/10.1080/15459624.2017.1339165
Oliveira, M., et al. (2009). The effects of meteorological factors on airborne fungal spore concentration in two areas differing in urbanisation level. International Journal of Biometeorology, 53(1), 61–73. https://doi.org/10.1007/s00484-008-0191-2
Onofre., L. H. F. S. B. (2010). DETERMINAÇÃO DA PRESENÇA DE FUNGOS ANEMÓFILOS E LEVEDURAS EM UNIDADE DE SAÚDE DA CIDADE DE FRANCISCO BELTRÃO- PR, pp. 22–26
Parsi, Z., & Grecki, T. (2006). Determination of ergosterol as an indicator of fungal biomass in various samples using non-discriminating flash pyrolysis. Journal of Chromatography A, 1130, 145–150. https://doi.org/10.1016/j.chroma.2006.07.045
Pescott, O. L., et al. (2015). Air pollution and its effects on lichens, bryophytes, and lichen-feeding Lepidoptera: Review and evidence from biological records. Biological Journal of the Linnean Society, 115(3), 611–635. https://doi.org/10.1111/bij.12541
Pöschl, U. (2005). Atmospheric aerosols: Composition, transformation, climate and health effects. Angewandte Chemie - International Edition, 44(46), 7520–7540. https://doi.org/10.1002/anie.200501122
Rackes, A., & Waring, M. S. (2013). Modeling impacts of dynamic ventilation strategies on indoor air quality of offices in six US cities. Building and Environment. https://doi.org/10.1016/j.buildenv.2012.10.013
Recio, R., et al. (2019). Picture of a Microorganism Trichoderma longibrachiatum: an unusual pathogen of fungal pericarditis. Clinical Microbiology and Infection. https://doi.org/10.1016/j.cmi.2019.02.006
Ristic, S., et al. (2017). Lichens as biological indicators of air quality in the urban area of Kursumlija (Southern Serbia). Kragujevac Journal of Science, 39, 165–175. https://doi.org/10.5937/kgjsci1739165r
Rosenfeld, D., et al. (2008). Flood or drought: How do aerosols affect precipitation? Science. https://doi.org/10.1126/science.1160606
Roy, S., & Gupta Bhattacharya, S. (2020). ‘Airborne fungal spore concentration in an industrial township: Distribution and relation with meteorological parameters. Aerobiologia, 36(4), 575–587. https://doi.org/10.1007/s10453-020-09653-9
Schmidt, S. K., et al. (2014). Do bacterial and fungal communities assemble differently during primary succession? Molecular Ecology. https://doi.org/10.1111/mec.12589
Schoenlein-crusius, I. H. et al. (2001). AIRBORNE FUNGI IN THE REGION OF CUBATÃO, SÃO PAULO STATE, BRAZI, pp. 61–65
Stamenković, S., et al. (2016). Air quality lichen monitoring at three selected urban areas in the Southern Serbia. Biologica NYSSANA, 7(September), 19–29. https://doi.org/10.5281/zenodo.159100
Stathakis, A., et al. (2015). Penicillium marneffei infection in a lung transplant recipient. Transplant Infectious Disease, 17(3), 429–434. https://doi.org/10.1111/tid.12377
Sterflinger, K., Tesei, D., & Zakharova, K. (2012). Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecology, 5(4), 453–462. https://doi.org/10.1016/J.FUNECO.2011.12.007
Temperini, C. V., et al. (2019). Diversity and abundance of airborne fungal spores in a rural cold dry desert environment in Argentinean Patagonia. Science of the Total Environment, 665, 513–520. https://doi.org/10.1016/j.scitotenv.2019.02.115
Theotônio, P. et al. (2007).‘O PAPEL DAS PARTÍCULAS DE AEROSSOL NO FUNCIONAMENTO DO ECOSSISTEMA AMAZÔNICO, Mudanças climáticas/ Artigos, pp. 48–50
Tiwari, P., Misra, B. N., & Sangwan, N. S. (2013). í µí»½-glucosidases from the fungus trichoderma: an efficient cellulase machinery in biotechnological applications. BioMed Research International. https://doi.org/10.1155/2013/203735
World Health Organization. (2003). Climate Change and Human Health - Risks and Responses Summary, pp. 1–37
Yamamoto, N., et al. (2012). Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air. The ISME Journal, 6(10), 1801–1811. https://doi.org/10.1038/ismej.2012.30
Yao, M. (2018). Bioaerosol: A bridge and opportunity for many scientific research fields. Journal of Aerosol Science, 115, 108–112. https://doi.org/10.1016/j.jaerosci.2017.07.010
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Dulcilena de Matos Castro e Silva contributed to conceptualization, methodology, investiagtion, resources, data curation, writing—original draft preparation, writing—review and editing, and project administration; Fábio Luiz Teixeira Gonçalves contributed to conceptualization, supervision, and funding acquisition; Rosa Maria Nascimento Marcusso contributed to software and data curation; Maria Regina Alves Cardoso contributed to validation and writing—review and editing; and Valter Batista Duo Filho contributed to resources, data curation, and writing—review and editing. All authors have read and agreed to the published version of the manuscript.
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de Matos Castro e Silva, D., Duo Filho, V.B., Marcusso, R.M.N. et al. Analyses of culturable microorganisms and chemical pollutants in the air of urban and rural areas in the region of São Paulo, Brazil. Aerobiologia (2024). https://doi.org/10.1007/s10453-024-09823-z
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DOI: https://doi.org/10.1007/s10453-024-09823-z