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Diversity of airborne Cladosporium species isolated from agricultural environments of northern Argentinean Patagonia: molecular characterization and plant pathogenicity

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Abstract

Fungal spores are normal components of external environments. They have been reported to be associated with human, animal and plant diseases causing primary and opportunistic infections. Cladosporium is commonly the most frequently isolated genus from air samples, and its species are considered mainly saprophytic, but there is a wide variety of taxa that can cause adverse effects on human and animal health and also on plants. In this work, we aimed to record Cladosporium spores frequency of isolation in northern Argentinean Patagonia and to perform a molecular characterization based on actin gene complemented with EF1α and ITS genes. The ability of the pathogens to cause disease in pip fruits of Packham’s Triumph and Abate Fetel pears and red delicious apples was determined. Results confirmed Cladosporium spores as the main genera isolated from air samples, and the molecular characterization revealed the existence of 11 species in this region grouped in C. cladosporioides and C. herbarum complexes. Pathogenicity tests revealed that Cladosporium sp. cause disease on fruit. Abate Fetel was the most susceptible to infection. These results compose the first study in Argentina in respect of identification at species level of airborne Cladosporium spores, and furthermore, it is the first report in northern Patagonia and the high valley of Río Negro productive region. This knowledge can help farmers to take preventive measures in order to avoid biological damage.

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References

  • Abdel Hameed, A. A., Khoder, M. I., Yuosra, S., Osman, A. M., & Ghanem, S. (2009). Diurnal distribution of airborne bacteria and fungi in the atmosphere of Helwan area, Egypt. Science of the Total Environment, 407, 6217–6222.

    Article  CAS  Google Scholar 

  • Aira, M. J., Rodríguez-Rajo, F. J., Fernández-González, M., Seijo, C., Elvira-Rendueles, B., Gutiérrez-Bustillo Abreu, I., et al. (2012). Cladosporium airborne spore incidence in the environmental quality of the Iberian Peninsula. Grana, 51(4), 293–304.

    Article  Google Scholar 

  • Al-Doory, Y., & Domson, J. F. (1984). Mould allergy. Philadelphia, PA: Lea and Febiger.

    Google Scholar 

  • Alhussaini, M. S., Moslem, M. A., Alghonaim, M. I., Al-Ghanayem, A. A., & Hefny, H. M. (2015). Biological studies on airborne Cladosporium species isolated from Riyadh City. Life Science Journal, 12(6), 83–91.

    Google Scholar 

  • Andersen, B., Kroger, E., & Roberts, R. (2002). Chemical and morphological segregation of Alternaria arborescens, A. infectoria and A. tenuissima species-groups. Mycological Research, 106(2), 170–182.

    Article  CAS  Google Scholar 

  • Aríngoli, E. E., Basílico, M. Z., Altahus, R. L., & Basílico, J. C. (2008). Multivariate analysis of fungal associations in the indoor air of Argentinean houses. International Biodeterioration and Biodegradation, 62, 281–286.

    Article  Google Scholar 

  • Artac, H., Kizilpinar, I., Pekcan, S., Dogan, C., & Reisli, I. (2009). Alternaria and Cladosporium spores in the atmosphere of Konya, Turkey. Allergy: European Journal of Allergy and Clinical Immunology, 64, 248–249.

    Google Scholar 

  • Benbow, J. M., & Sugar, D. (1999). Fruit surface colonization and biological control of postharvest diseases of pear by preharvest yeast applications. Plant Disease, 83, 839–844.

    Article  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 

  • Bensch, K., Groenewald, J. Z., Dijksterhuis, J., Starink-Willemse, M., Andersen, B., Shin, H.-D., et al. (2010). Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Studies in Mycology, 67, 1–94.

    Article  CAS  Google Scholar 

  • Braun, U. (2003). Miscellaneous notes on some cercosporoid hyphomycetes. Bibliotheca Lichenologica, 86, 79–98.

    Google Scholar 

  • Bueno, D. J., Silva, J. O., & Oliver, G. (2003). Hongos ambientales en una biblioteca: un año de estudio. Anales de Documentación, 6, 27–34.

    Google Scholar 

  • Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia, 91, 553–556.

    Article  CAS  Google Scholar 

  • Cvetnic, Z., & Pepelnjak, S. (1997). Distribution and mycotoxin-producing ability of some fungal isolates from the air. Atmospheric Environment, 31, 491–495.

    Article  CAS  Google Scholar 

  • Domsch, K. H., Gams, W., & Anderson, T. H. (1980). Compendium of soil fungi (Vols. 1 & 2). London: Academic Press.

  • Dugan, F. M., Braun, U., Groenewald, J. Z., & Crous, P. W. (2008). Morphological plasticity in Cladosporium sphaerospermum. Persoonia, 21, 9–16.

    Article  CAS  Google Scholar 

  • Dugan, F. M., Schubert, K., & Braun, U. (2004). Check-list of Cladosporium names. Schlechtendalia, 11, 1–103.

    Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  Google Scholar 

  • Erkara, I. P., Asan, A., Yilmaz, V., Pehlivan, S., & Okten, S. S. (2008). Airborne Alternaria and Cladosporium species and relationship with meteorological conditions in Eskisehir City, Turkey. Environmental Monitoring and Assessment, 144(1), 31–41.

    Article  Google Scholar 

  • Fang, Z., Ouyang, Z., Hu, L., Wang, X., Zheng, H., & Lin, X. (2005). Culturable airborne fungi in outdoor environments in Beijing, China. Science of the Total Environment, 350, 47–58.

    Article  CAS  Google Scholar 

  • Greco, M., Kemppainen, M., Pose, G., & Pardo, A. (2015). Taxonomic characterization and secondary metabolite profiling of Aspergillus section Aspergillus contaminating feeds and feedstuffs. Toxins, 7(9), 3512–3537.

    Article  CAS  Google Scholar 

  • Grinn-Gofroń, A., Strzelczak, A., & Wolski, T. (2011). The relationships between air pollutants, meteorological parameters and concentration of airborne fungal spores. Environmental Pollution, 159, 602–608.

    Article  Google Scholar 

  • Kulko, A. B., & Marfenina, O. E. (2001). Distribution of microscopic fungi along Moscow roads. Mikrobiologia, 70, 709–771.

    CAS  Google Scholar 

  • Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.

    Article  CAS  Google Scholar 

  • Lee, T., Grinshpun, S. A., Martuzevicius, D., Adhikari, A., Crawford, C. M., & Reponen, T. (2006). Culturability and concentration of indoor and outdoor airborne fungi in six single-family homes. Atmospheric Environment, 40, 2902–2910.

    Article  CAS  Google Scholar 

  • Lutz, C. M., Sosa, C. M., & Colodner, A. (2016). Effect of pre and postharvest application of fungicides on postharvest decay of Bosc pear caused by Alternaria-Cladosporium complex in North Patagonia. Argentina: Scientia Horticulturae. https://doi.org/10.1016/j.scienta.2017.05.007.

    Book  Google Scholar 

  • Mitakakis, T. Z., & Guest, D. I. (2001). A fungal spore calendar for the atmosphere of Melbourne, Australia, for the year 1993. Aerobiologia, 17, 171–176.

    Article  Google Scholar 

  • Muhsin, T. M., & Adlan, M. M. (2012). Seasonal distribution pattern of outdoor airborne fungi in Basrah city, southern Iraq. Journal of Basrah Researches, 38(1A), 90–98.

    Google Scholar 

  • Mullins, J. (2001). Microorganisms in outdoor air. In R. A. Samson & J. D. Miller (Eds.), Microorganisms in home and indoor work environments: Diversity, health impacts, investigation and control (flannigan B (pp. 3–16). London: Taylor and Francis.

    Google Scholar 

  • Park, H. G., Managbanag, J. R., Stamenova, E. K., & Jong, S. C. (2004). Comparative analysis of common indoor Cladosporium species based on molecular data and conidial characters. Mycotaxon, 89(2), 441–451.

  • Park, Y. S., Kim, K. C., Lee, J. H., Cho, S. M., Choi, Y. S., & Kim, Y. C. (2008). Cladosporium sp. is the major causal agent in the microbial complex associated with the skin sooty dapple disease of the asian pear in Korea. The Plant Pathology Journal, 24(2), 118–124.

  • Pitt, J., & Hocking, A. (2009). Fungi and food spoilage (3rd ed.). New York, NY: Springer.

    Book  Google Scholar 

  • Robbins, C. A., Swenson, L. J., Nealley, M. L., Gots, R. E., & Kelman, B. J. (2000). Health effects of mycotoxins in indoor air: A critical review. Applied Occupational and Environmental Hygiene, 15, 773–784.

    Article  CAS  Google Scholar 

  • Rodríguez, A., & Muñoz, A. (2006). Síntesis Agrometeorológica para el período 1990-2004. EEA Alto Valle. Ed. INTA. Boletín Divulgación Técnica, (53), 38.

  • Samson, R., Hoekstra, E., Frisvad, J., & Filtenborg, O. (2000). Introduction to food- and airborne fungi (6ª ed.). Utrecht: Centraalbureau Voor Schímmelcultures.

    Google Scholar 

  • Sandoval-Denis, M., Sutton, D. A., Martin-Vicente, A., Cano-Lira, J. F., Wiederhold, N., Guarro, J., et al. (2015). Cladosporium species recovered from clinical samples in the United States. Journal of Clinical Microbiology, 53, 2990–3000. https://doi.org/10.1128/JCM.01482-1.

    Article  CAS  Google Scholar 

  • Schubert, K., Groenewald, J. Z., Braun, U., Dijksterhuis, J., Starink, M. S., Hill, C. F., et al. (2007). Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Studies in Mycology, 58, 105–156.

    Article  CAS  Google Scholar 

  • Shelton, B. G., Kirkland, K. H., Flanders, W. D., & Morris, G. K. (2002). Profiles of airborne fungi in buildings and outdoor environments in the United States. Applied and Environmental Microbiology, 68, 1743–1753.

    Article  CAS  Google Scholar 

  • Sindt, C., Besancenot, J. P., & Thibaudon, M. (2016). Airborne Cladosporium fungal spores and climate change in France. Aerobiologia, 32(1), 53–68.

    Article  Google Scholar 

  • Sugar, D., & Powers, K. (1986). Interactions among fungi causing postharvest decay of pear. Plant Disease, 70, 1132–1134.

    Article  Google Scholar 

  • Tournas, V. H. (2005). Spoilage of vegetable crops by bacteria and fungi and related health hazards. Critical Reviews in Microbiology, 31, 33–44.

    Article  CAS  Google Scholar 

  • Verhoeff, A. P., Van Wijnen, J. H., Boleij, J. S. M., Brunekreef, B., Van Reenen-Hoekstra, E. S., & Samson, R. A. (1990). Enumeration and identification of airborne viable mould propagules in houses. Allergy, 45, 275–284.

    Article  CAS  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR Protocols: A guide to methods and applications (Innis MA (pp. 315–322). San Diego, CA: Academic Press.

    Google Scholar 

  • Zalar, P., de Hoog, G. S., Schroers, H.-J., Crous, P. W., Groenewald, J. Z., & Gunde-Cimerman, N. (2007). Phylogeny and ecology of the ubiquitous saprobe Cladosporium sphaerospermum, with descriptions of seven new species from hypersaline environments. Studies in Mycology, 58, 157–183.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge Javier Alonso (Universidad Nacional de Río Negro), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional de Río Negro (UNRN) (Grant No. PI 40-A-382) and Universidad Nacional de Quilmes (UNQ) for financial support.

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  1. Escuela de Producción, Tecnología y Medio Ambiente, Universidad Nacional de Río Negro and Consejo Nacional de Investigaciones Científicas y Técnicas, Mitre 331, 8336, Villa Regina, Provincia de Río Negro, Argentina

    Carolina Virginia Temperini & Graciela Noemí Pose

  2. Laboratorio de Micología Molecular, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas, Roque Saenz Peña 352, B1876BXD, Bernal, Provincia de Buenos Aires, Argentina

    Alejandro Guillermo Pardo

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  1. Carolina Virginia Temperini
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Correspondence to Carolina Virginia Temperini.

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Temperini, C.V., Pardo, A.G. & Pose, G.N. Diversity of airborne Cladosporium species isolated from agricultural environments of northern Argentinean Patagonia: molecular characterization and plant pathogenicity. Aerobiologia 34, 227–239 (2018). https://doi.org/10.1007/s10453-018-9509-7

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