Identification and Characterization of Fungi Isolated from a Cheese Cave in the Eastern United States
DOI:
https://doi.org/10.55632/pwvas.v95i3.1018Keywords:
indoor fungi, cheese fungi, PenicilliumAbstract
Fungal spores are ubiquitous in indoor air, with the diversity of species geographically variable. Species present depend upon outdoor sources, physical conditions of the built environment, and human use of the built environment. Cheese is a microbial product produced through inoculation of milk with specific fungal and bacterial cultures. Indigenous fungi can also impact cheese flavor and quality. While there are studies investigating the microbiome of cheese and starter cultures, there are not many studies investigating the airborne fungal community in cheese caves. This study investigated the viable airborne fungi present in a man-made cheese cave in the Eastern United States. Fungi were captured passively on both general culture media and milk-based media using the open plate method. Thirty-one isolates were identified to genus by sequence of the nuclear ribosomal internal transcribed spacer (ITS) region. Most of the isolates were cheese-associated taxa: Penicillium (26 isolates) and Scopulariopsis (1 isolate). The only other taxon identified was Cladosporium (4 isolates), which is commonly isolated in surveys of both indoor and outdoor air and has been isolated from cheese. The airborne Penicillium-Fasciculata isolates captured from the cheese cave exhibit growth traits (conidiation, increased growth on malt extract media, and loss of casein hydrolysis) more similar to wild Penicillium fungi than the domesticated commercial cheese strain Penicillium candidum.
References
Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. The ISME Journal, 7(7), 1262–1273. https://doi.org/10.1038/ismej.2013.28
Bensch, K., Groenewald, J. Z., Meijer, M., Dijksterhuis, J., Jurjević, Andersen, B., Houbraken, J., Crous, P. W., & Samson, R. A. (2018). Cladosporium species in indoor environments. 89, 177–301. https://doi.org/10.1016/J.SIMYCO.2018.03.002
Beresford, T. P., Fitzsimons, N. A., Brennan, N. L., & Cogan, T. M. (2001). Recent advances in cheese microbiology. International Dairy Journal, 11(4–7), 259–274. https://doi.org/10.1016/S0958-6946(01)00056-5
Boutrou, R., & Guéguen, M. (2005). Interests in Geotrichum candidum for cheese technology. International Journal of Food Microbiology, 102(1), 1–20. https://doi.org/10.1016/j.ijfoodmicro.2004.12.028
Dieuleveux, V., Van Der Pyl, D., Chataud, J., & Gueguen, M. (1998). Purification and Characterization of Anti-Listeria Compounds Produced by Geotrichum candidum. Applied and Environmental Microbiology, 64(2), 800. https://doi.org/10.1128/AEM.64.2.800-803.1998
Flannigan, B., Samson, R. A., & Miller, J. D. (Eds.). (2011). Microorganisms in Home and Indoor Work Environments: Diversity, Health Impacts, Investigation and Control (Second). CRC Press. https://doi.org/https://doi.org/10.1201/b10838
Fradkin, A., Tarlo, S. M., Tobin, R. S., Tucic-Porretta, M., & Malloch, D. (1987). Species identification of airborne molds and its significance for the detection of indoor pollution. JAPCA, 37(1), 51–53. https://doi.org/10.1080/08940630.1987.10466201
Garnier, L., Valence, F., & Mounier, J. (2017). Diversity and Control of Spoilage Fungi in Dairy Products: An Update. Microorganisms, 5(3). https://doi.org/10.3390/microorganisms5030042
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98. https://www.academia.edu/download/29520866/1999hall1.pdf
Janssen, R. H. H., Heald, C. L., Steiner, A. L., Perring, A. E., Alex Huffman, J., Robinson, E. S., Twohy, C. H., & Ziemba, L. D. (2021). Drivers of the fungal spore bioaerosol budget: Observational analysis and global modeling. Atmospheric Chemistry and Physics, 21(6), 4381–4401. https://doi.org/10.5194/ACP-21-4381-2021
Kandasamy, S., Park, W. S., Yoo, J., Yun, J., Kang, H. B., Seol, K.-H., Oh, M.-H., & Ham, J. S. (2020). Characterisation of fungal contamination sources for use in quality management of cheese production farms in Korea. Asian-Australasian Journal of Animal Sciences, 33(6), 1002–1011. https://doi.org/10.5713/ajas.19.0553
Kure, C. F., & Skaar, I. (2019). The fungal problem in cheese industry. Current Opinion in Food Science, 29, 14–19. https://doi.org/https://doi.org/10.1016/j.cofs.2019.07.003
Lee, B. G., Yang, J. I. L., Kim, E., Geum, S. W., Park, J. H., & Yeo, M. K. (2021). Investigation of bacterial and fungal communities in indoor and outdoor air of elementary school classrooms by 16S rRNA gene and ITS region sequencing. Indoor Air, 31(5), 1553–1562. https://doi.org/10.1111/INA.12825
Li, D.-W., & Kendrick, B. (1995). A year-round comparison of fungal spores in indoor and outdoor air. Mycologia, 87(2), 190–195. https://doi.org/10.1080/00275514.1995.12026520
Lücking, R., Aime, M. C., Robbertse, B., Miller, A. N., Ariyawansa, H. A., Aoki, T., Cardinali, G., Crous, P. W., Druzhinina, I. S., Geiser, D. M., Hawksworth, D. L., Hyde, K. D., Irinyi, L., Jeewon, R., Johnston, P. R., Kirk, P. M., Malosso, E., May, T. W., Meyer, W., … Schoch, C. L. (2020). Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus, 11(1), 24. https://doi.org/10.1186/S43008-020-00033-Z
Martin, J. G. P., & Cotter, P. D. (2023). Filamentous fungi in artisanal cheeses: A problem to be avoided or a market opportunity? Heliyon, 9(4), e15110. https://doi.org/10.1016/j.heliyon.2023.e15110
Nevalainen, A., Täubel, M., & Hyvärinen, A. (2015). Indoor fungi: Companions and contaminants. Indoor Air, 25(2), 125–156. https://doi.org/10.1111/INA.12182
Ren, P., Jankun, T. M., & Leaderer, B. P. (1999). Comparisons of seasonal fungal prevalence in indoor and outdoor air and in house dusts of dwellings in one Northeast American county. Journal of Exposure Analysis and Environmental Epidemiology, 9(6), 560–568. https://doi.org/10.1038/sj.jea.7500061
Ropars, J., Cruaud, C., Lacoste, S., & Dupont, J. (2012). A taxonomic and ecological overview of cheese fungi. International Journal of Food Microbiology, 155(3), 199–210. https://doi.org/10.1016/J.IJFOODMICRO.2012.02.005
Ropars, J., Didiot, E., Rodríguez de la Vega, R. C., Bennetot, B., Coton, M., Poirier, E., Coton, E., Snirc, A., Le Prieur, S., & Giraud, T. (2020). Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties. Current Biology, 30(22), 4441-4453.e4. https://doi.org/10.1016/j.cub.2020.08.082
Salque, M., Bogucki, P. I., Pyzel, J., Sobkowiak-Tabaka, I., Grygiel, R., Szmyt, M., & Evershed, R. P. (2012). Earliest evidence for cheese making in the sixth millennium bc in northern Europe. Nature 2012 493:7433, 493(7433), 522–525. https://doi.org/10.1038/nature11698
Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., Chen, W., Bolchacova, E., Voigt, K., Crous, P. W., Miller, A. N., Wingfield, M. J., Aime, M. C., An, K. D., Bai, F. Y., Barreto, R. W., Begerow, D., Bergeron, M. J., Blackwell, M., … Schindel, D. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America, 109(16), 6241–6246. https://doi.org/10.1073/PNAS.1117018109/SUPPL_FILE/SD01.XLS
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(4), 1743–1753. https://doi.org/10.1128/AEM.68.4.1743-1753.2002
Steensels, J., Gallone, B., Voordeckers, K., & Verstrepen, K. J. (2019). Domestication of Industrial Microbes. Current Biology, 29(10), R381–R393. https://doi.org/10.1016/j.cub.2019.04.025
Visagie, C. M., Hirooka, Y., Tanney, J. B., Whitfield, E., Mwange, K., Meijer, M., Amend, A. S., Seifert, K. A., & Samson, R. A. (2014). Aspergillus, Penicillium and Talaromyces isolated from house dust samples collected around the world. Studies in Mycology, 78, 63–139. https://doi.org/10.1016/j.simyco.2014.07.002
Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S. B., Klaassen, C. H. W., Perrone, G., Seifert, K. A., Varga, J., Yaguchi, T., & Samson, R. A. (2014). Identification and nomenclature of the genus Penicillium. Studies in Mycology, 78(1), 343–371. https://doi.org/10.1016/J.SIMYCO.2014.09.001
Woudenberg, J. H. C., Meijer, M., Houbraken, J., & Samson, R. A. (2017). Scopulariopsis and scopulariopsis-like species from indoor environments. 88. https://doi.org/10.1016/J.SIMYCO.2017.03.001
Downloads
Published
How to Cite
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Proceedings of the West Virginia Academy of Science applies the Creative Commons Attribution-NonCommercial (CC BY-NC) license to works we publish. By virtue of their appearance in this open access journal, articles are free to use, with proper attribution, in educational and other non-commercial settings.
