Airborne microorganisms in gypsum maze caves of the western Ukraine : biodiversity and geoecological control

• Autorzy: Wojkowski Jakub , Andreychouk Viacheslav , Frączek Krzysztof

Identyfikatory

DOI

10.7306/gq.1765

• Języki publikacji: EN

Abstrakty

EN

Microbiological and microclimatic studies of two giant gypsum caves in Bukovina (Prypruttia) and Podillya, Ukraine, have characterized the microbial air quality and the microclimate within them, via stationary air sampling using the volumetric (impact) method. Dominant species of bacteria and fungi were identified by MALDI-TOF mass spectrometry by comparing the mass spectra of ribosomal proteins (molecular fingerprints) with the spectra in a database. Basic meteorological elements such as air temperature, air humidity, and airflow velocity were measured. Bacterial aerosol concentrations ranged from 37 to 232 CFU . m^–3 in the indoor air of the caves, and for fungi from 10 to 365 CFU . m^–3. The range of bacterial aerosol concentrations in the outdoor environment ranged from 140 to 535 CFU . m^–3, being significantly higher than inside the caves. The most common microorganisms in the cave air were mesophilic Gram-positive cocci (Staphylococcus), non-spore-forming Gram-positive rods (Arthrobacter and Rhodococcus) as well as Bacillus and Lactobacillus, mesophilic actinobacteria (Streptomyces) and filamentous fungi (Alternaria, Penicillium). The microclimatic measurements carried out in both caves testify to the high stability of temperature and humidity. Measurements made using the katathermometric method showed that the speed of air movement in the static part of both caves ranges between 0.01 and 0.03 m . s^–1. The stability of the microclimatic conditions of the cave interior suggests that most microorganisms come from outside and enter the caves during an exchange of air with the external environment. In general, the concentration of microorganisms in the air of these caves is characterized by significant spatial variation within the cave fields but clearly tends to decrease as one moves away from the cave entrance. Our study shows that the content of airborne microorganisms and their spatial distribution in caves are determined by both external factors and the environment of the caves’ interior, especially microclimatic, morphometric and morphological factors such as the cave volume, size of the chambers and corridors and maze structure.

Słowa kluczowe

EN

biospeleology; aerobiology; bioaerosol; airborne microorganisms; cave microclimate

• Wydawca: Państwowy Instytut Geologiczny - Państwowy Instytut Badawczy
• Czasopismo: Geological Quarterly
• Rocznik: 2024
• Tom: Vol. 68, No. 4
• Strony: art. no. 37
• Opis fizyczny: Bibliogr. 62 poz., fot., rys., tab., wykr.

Twórcy

autor

Wojkowski Jakub

• University of Agriculture in Kraków, Department of Ecology, Climatology and Air Protection, Mickiewicza 24/28, 30-059 Kraków, Poland

• https://orcid.org/0000-0003-1115-1755

autor

Andreychouk Viacheslav

• Akademia Bialska im. Jana Pawła II, Sidorska 95/97, 21-500 Biała Podlaska, Poland

• https://orcid.org/0000-0002-9656-4542

autor

Frączek Krzysztof

• University of Agriculture in Kraków, Department of Microbiology and Biomonitoring, Mickiewicza 24/28, 30-059 Kraków, Poland

• https://orcid.org/0000-0002-0788-6292

Bibliografia

• 1. Andreychouk, V., 2007. Peshchera Zoloushka (in Russian). Sosnoviec-Simferopol, 407.
• 2. Andreychouk, V., 2016. Columned halls as a stage in morphological development of maze caves. Acta Geographica Silesiana, 23: 11-17.
• 3. Andreychouk, V., Klimchouk, A., 2001. Geomicrobiology and redox geochemistry of the karstified Miocene gypsum aquifer, western Ukraine. The study from Zoloushka Cave. Geomicrobiology, 18: 275-295.
• 4. https://doi.org/10.1080/01490450152467796 Andreychouk, V., Klimchouk, A., 2017. Zoloushka Cave (Ukraine-Moldova) - a prime example of hypogene artesian speleogenesis in gypsum. In: Hypogene Karst Regions and Caves of the World (eds. A. Klimchouk, A. Palmer, J. Waele, A. Auler and F. Audra): 387-406. Springer. https://doi.org/10.1007/978-3-319-53348-3 24
• 5. Andreychouk, V., Klimchouk, A., Boston, P., Galuskin, E., 2009. Unique iron-manganese colonies of microorganisms in Zoloushka Cave (Ukraine-Moldova) (in Russian). Speleology and Karstology, 3: 5-25.
• 6. Andreychouk, V., Teleshman, I., Kuprich, P., 2011. Prostra- nstvenno-dinamicheskiye osobennosti raspredeleniya CO2 v vozduche peshchery Zoloushka (in Russian). Speleologia i Karstologia, 7: 15-25.
• 7. Andreychouk, V., Różkowski, J., Jóźwiak, J., 2021. Variability in chemical composition of waters in the Zoloushka gypsum cave (Ukraine-Moldova) as a consequence of anthropogenic degradation of a karst aquifer. Geological Quarterly, 65, 41. https://doi.org/10.7306/gq.1610
• 8. Bastian, F., Jurado, V., Nováková, A., Alabouvette, C., Saiz-Jimenez, C., 2010. The microbiology of Lascaux Cave. Microbiology, 156: 644-652. https://doi.org/10.1099/mic.0.036160-0
• 9. Chmiel, D., Mickowska, B., 2002. Systemy regulatorowe agr i sar u Staphylococcus aureus (in Polish). Postępy Biologii Komórki, 29: 103-120.
• 10. Docampo, S., Mar Trigo, M., Recio, M., Melgar, M., García- -Sánchez, J., Cabezudo, B., 2011. Fungal spore content of the atmosphere of the Cave of Nerja (southern Spain): diversity and origin. Science of the Total Environment, 409: 835-843. https://doi.org/1016/i.scitotenv.2010.10.048
• 11. Dominguez-Monino, I., Jurado, V., Rogerio-Candelera, M.A., Hermosin, B., Jimenez, C.S., 2021. Airborne fungi in show caves from southern Spain. Applied Sciences, 11: 5027. https://doi.org/10.3390/app11115027
• 12. Douwes, J., Thorne, P., Pearce, N., Heederik, D., 2003. Bioaerosol health effects and exposure assessment: progress and prospects. Annals of Occupational Hygiene, 47: İ87-200.
• 13. Duan, Y., Wu, F., He, D., Gu, J-D., Feng, H., Chen, T., Liu, G., Wang, W., 2021. Diversity and spatial - temporal distribution of airborne fungi at the world culture heritage site Maijishan Grottoes in China. Aerobiologia, 37: 681-694. https://doi.org/10.1007/s10453-021-09713-8
• 14. Epure, L., Muntean, V., Constantin, S., Moldovan, O.T., 2017. Ecophysiological groups of bacteria from cave sediments as potential indicators of paleoclimate. Quaternary International, 432: 20-32. https://doi.org/10.1016/i.quaint.2015.04.016
• 15. Flannigan, B., Samson, RA., Miller, J.D. eds., 2001. Microorganisms in Home and Indoor Work Environments. Taylor and Francis, New York.
• 16. Garcia-Anton, E., Cuezva, S., Jurado, V., Porca, E., Miller, A.Z., Fernandez-Cortes, A., Saiz-Jimenez, C., Sanchez-Moral, S., 2013. Combining stable isotope (13C) of trace gases and aerobiological data to monitor the entry and dispersion of microorganisms in caves. Environmental Sciences and Pollution Research, 21:473-484. https://doi.org/10.1007/s11356-013-1915-3
• 17. Ghosh, S., Kuisiene, N., Cheeptham, N. 2017. The cave microbiome as a source for drug discovery: Reality or pipe dream? Biochemical Pharmacology, 134: 18-34.
• 18. Gottstein Matocec, S. ed., 2002. An overview of the cave and interstitial biota of Croatia. Natura Croatica, 11: 1-112.
• 19. Górny, R.L., Mainelis, G., Grinshpun, S.A., Willeke, K., Dutkiewicz, J., Reponen, T., 2003. Re i ease of Streptomyces albus propagules from contaminated surfaces. Environmental Research, 91:45-53. https://10.1016/s0013-9351(02)00006-3
• 20. Gradziński, M., Chmiel, M.J., Motyka, J., 2012. Formation of calcite by chemolithoautotrophic bacteria - a new hypothesis, based on microcrystalline cave pisoids. Annales Societatis Geologorum Poloniae, 82: 361-369.
• 21. Jones, A.M., Harrison, R.M., 2004. The effects of meteorological factors on at mospheric bioaerosol concentrations - a review. Science of the Total Environment, 326: 151-180. https://doi.org/10.1016/i.scitotenv.2003.11.021
• 22. Jurado, V., Porca, E., Cuezva, S., Fernandez-Cortes, A., Sanchez-Moral, S., Saiz-Jimenez, C., 2010. Fungal outbreak in a show cave. Science of the Total Environment, 408: 3632-3638. https://doi.org/10.1016/i.scitotenv.2010.04.057
• 23. Klimchouk, A., Andreychouk, V., 2017. Gypsum Karst in the southwest outskirts of the Eastern European Platform (Western Ukraine): a type region of artesian transverse speleogenesis. In: Hypogene Karst Regions and Caves of the World (eds. A. Klimchouk, A. Palmer, J. Waele, A. Auler and J. Audra): 363-387. Springer. https://doi.org/10.1007/978-3-319-53348-3 24
• 24. Lepinay, C., Mihajlovski, A., Touron, S., Seyer, D., Bousta, F., Di Martino, P., 2018. Bacterial diversity associated with saline efflorescences damaging the walls of a French decorated prehistoric cave registered as a World Cultural Heritage Site. International Biodeterioration and Biodegradation, 130: 55-64. https://doi.org/10.1016/i.ibiod.2018.03.016
• 25. Libudzisz, Z., Kowal, K., Żakowska, Z., 2009. Mikrobiologia techniczna. Mikroorganizmy i środowiska ich występowania (in Polish). Wydawnictwo Naukowe PWN, Warszawa.
• 26. Lis, D.O., Ulfig, K., Wlazlo, A., Pastuszka, J.S., 2004. Microbial air quality in offices at municipal landfills. Journal of Occupational and Environmental Hygiene, 1: 62-68.
• 27. Macher, J. ed., 1999. Bioaerosols: assessment and control. American Conference of Governmental Industrial Hygienists, Cincinnati.
• 28. Marcinowska, K., 2002. Characteristic, Occurrence and Importance of Actinomycetales in Nature. Microorganisms' Activity in Various Environments. Academy of Agriculture, Kraków.
• 29. Martin-Sanchez, P.M., Jurado, V., Porca, E., Bastian, F., Lacanette, D., Alabouvette, C., Saiz-Jimenez, C., 2014. Airborne microorganisms in Lascaux Cave (France). International Journal of Speleology, 43: 295-303. https://doi.org/10.5038/1827-806X.43.3.6
• 30. Martin-Sanchez, P.M., Miller, A., Saiz-Jimenez, C., 2015. Lascaux Cave: an example of fragile ecological balance in subterranean environments. In: Microbial Life of Cave Systems (ed A. Summers Engel): 279-302. De Gruyter. https://doi.org/10.1515/9783110339888-015
• 31. Muhammad, Y., 2018. Analysis of bacterial communities and characterization of antimicrobial strains from cave microbiota. Brazilian Journal of Microbiology, 49: 248-257.
• 32. Mulec, J., Oarga, A., 2014. Ecological evaluation of air and water habitats in the Great Cavern of Santo Tomás, Cuba. Revista Mexicana de Biodiversidad, 85: 910-917.
• 33. Mulec, J., Krištůfek, V., Chroňáková, A., 2012. Comparative microbial sampling from eutrophic caves in Slovenia and Slovakia using RIDA®COUNT test kits. International Journal of Speleology, 41: 1-8.
• 34. Mulec, J., Oarga-Mulec, A., Šturm, S., Tomazin, R., Matos, T., 2017. Spacio-temporal distribution and tourist impact on airborne bacteria in a cave (Škocjan Caves, Slovenia). Diversity, 9: 28. https:// doi.org/10.3390/d9030028
• 35. Nakaew, N., Pathom-aree, W., Lumyong, S., 2009. Generic diversity of rare actinomycetes from Thai cave soils and their possible use as new bioactive compounds. Actinomycetologica, 23: 21-26.
• 36. Northup, D., Lavoie, K., 2001. Geomicrobiology of caves: a review. Geomicrobiology Journal, 18: 199-222.
• 37. Nováková, A., 2009. Microscopic fungi isolated from the Domica Cave system (Slovak Karst National Park, Slovakia). A review. International Journal of Speleology, 38: 71-82.
• 38. Nováková, A., Hubka, V., Saiz-Jimenez, C., 2014. Microscopic fungi isolated from cave air and sediments in the Nerja Cace - preliminary results. In: The Conservation of Subterranean Cultural Heritage (ed. C. Saiz-Jimenez): 239-245. CRC Press. https://doi.org/10.1201/b17570-29
• 39. Nováková, A., Kubátová, A., Sklenář, F., Hubka, V., 2018. Microscopic fungi on cadavers and skeletons from cave and mine environments. Czech Mycology, 70: 101-121.
• 40. Ogórek, R., 2016. Badania speleomykologiczne w Demianowskiej Jaskini Lodowej (Słowacja) (in Polish). Materiały 50. Sympozjum Speleologicznego. Kielce-Chęciny: 134-135.
• 41. Ogórek, R., 2018. Speleomycology of air in Demanovská Cave of Liberty (Slovakia) and new airborne species for fungal sites. Speleomycology of air in Demanovská Cave of Liberty (SLOvakia) and new airborne species for fungal sites. Journal of Cave and Karst Studies, 80: 153-160. https://doi.org/10.4311/2018MB0104
• 42. Ogórek, R., Lejman, A., 2013. Analiza mikologiczna powietrza w Jaskini Niedźwiedziej w Kletnie. Doniesienie wstępne (in Polish). “Episteme”, 18: 121-130.
• 43. Peryt, T.M., 1996. Sedimentology of Badenian (middle Miocene) gypsum in eastern Galicia, Podolia and Bukovina (West Ukraine). Sedimentology, 43: 571-588. https://doi.org/10.1046/i.1365-3091.1996.d01-26.x
• 44. Peryt, T.M., 2001. Gypsum facies transitions in basin-marginal evaporites: middle Miocene (Badenian) of west Ukraine. Sedimentology, 48: 1103-1119. https://doi.org/10.1046/i.1365-3091.2001.00410.x
• 45. Porca, E., Jurado, V., Martin-Sanchez, P.M., Hermosin, B., Bastian, F., Alabouvette, C., Saiz-Jimenez, C., 2011. Aerobiology: an ecological indicator for early detection and control of fungal outbreaks in caves. Ecological Indicators, 11: 1594-1598. https://doi.org/10.1016/j.ecolind.2011.04.003
• 46. Pusz, W., Ogórek, R., Knapik, R., Kozak, B., Bujak, H., 2015. The occurrence of fungi in the recently discovered Jarkowicka Cave in the Karkonosze Mts. (Poland). Geomicrobiology Journal, 32: 59-67. https ://doi.org/10.1080/01490451.2014.925010
• 47. Ren, M., Jones, B., Nie, X., Lin, X., Meng, C., 2024. Carbonate microbialites and chemotrophic microbes: insights from caves from south-east China. Sedimentology, 71: 1558-1590. https://doi.org/10.1111/sed.13185
• 48. Reponen, T.A., Gazenko, S.V., Grinshpun, S.A., Willeke, K., Cole, E.C., 1998. Characteristics of airborne actinomycete spores. Applied Environmental Microbiology, 64: 3807-3812. https://doi.org/10.1128/aem.64.10.3807-3812.1998
• 49. Sanchez-Moral, S., Jurado, V., Fernandez-Cortes, A., Cuezva, S., Martin-Pozas, T., Gonzalez-Pimentel, J.L., Ontanon, R., Saiz-Jimenez, C., 2021. Environment-driven control of fungi in subterranean ecosystems: the case of La Garma Cave (northern Spain). International Microbiology, 24: 573-591. https://doi.org/10.1007/s10123-021-00193-x
• 50. Sibson, R., 1981. A brief description of natural neighbour interpolation, interpolating multivariate data. In: Multivariate Data (ed. V Barnett): 21-36. New York: John Wiley and Sons.
• 51. Stańkowska, D., Kaca, W., 2005. Systemy komunikacji międzykomórkowej bakterii gram-ujemnych i ich znaczenie w ekspresji cech fenotypowych (in Polish). Postępy Mikrobiologii, 44: 99-111.
• 52. Sugita, T., Kikuchi, K., Makimura, K., Urata, K. Someya, T., Kamei, K., Niimi, M., Uehara, Y., 2005. Trichosporon species iso lated from guano samples obtained from bat-inhabited caves in Japan. Applied and Environmental Microbiology, 71: 7626-7629. https://doi.org/10.1128/AEM .71.11.7626-7629.2005
• 53. Taylor, E.L.S, Resende-Stoianoff, M.A.A., Lopes Ferreira, R., 2013. Mycological study for a management plan of a neotropical show cave (Brazil). International Journal of Speleology, 42: 267-277. https://doi.org/10.5038/1827-806X.42.3.10
• 54. Ukrainian Speleological Association, 2018. Ukrainian cave cadastre. http://www.speleoukraine.org/index.php/ru/peshcherv-ukrainv Ukrainian Speleological Association, 2021. Information and analytical system of the Ukrainian cave cadastre. https://caves.in.ua/cave.php7list
• 55. Vaughan, M., Angelini, P., Zacchi, L., 2000. The influence of human and animal visitation on the yeast ecology of three Italian caverns. Annals of Microbiology, 50: 133-140.
• 56. Vaughan, M.J., Maier, R.M., Pryor, B.M., 2011. Fungal communities on speleothem surfaces in Kartchner Caverns, Arizona, USA. International Journal of Speleology, 40: 65-77. https://doi.org/10.5038/1827-806X.40.1.8
• 57. Wang, W., Ma, X., Ma, Y., Mao, L., Wu, F., Ma, X., An, L., Feng, H., 2010. Seasonal dynamic of airborne fungi in different caves of the Mogao Grottoes. Dunhuang, China. International Biodeterioration and Biodegradation, 64: 461-466. https://doi.org/10.1016%2Fi.ibiod.2010.05.005
• 58. Wojkowski, J., 2013. Microclimate and microflora of caves of Ojców National Park (in Polish with English summary). Prace Muzeum Szafera, 23: 75-90.
• 59. Wojkowski, J., Andreychouk, V., Frączek, K., 2019. Airborne microorganisms of hypogenic maze caves based on the example of the Zoloushka Cave, Ukraine-Moldova. Annual Set The Environment Protection, 21: 1116-1135.
• 60. Zhang, Z.F., Liu, F., Zhou, X., Liu, X.Z., Liu, S.J., Cai, L., 2017. Culturable mycobiota from Karst caves in China, with descriptions of 20 new species. Persoonia, 39: 1-31.
• 61. Zhang, Z.F., Zhu, H.Z., Eurwilaichitr, L., Ingsriswang, S., Raza, M., Chen, Q., Zhao, P., Liu, F., Cai, L., 2020. Culturable mycobiota from Karst caves in China II, with descriptions of 33 new species. Fungal Diversity, 106. https://doi.org/10.1007/s13225-020-00453-7
• 62. Zhu, H-Z., Zhang, Z-F., Zhou, N., Jiang, C-Y., Wang, B-J., Cai, L., Wang, H-M., Liu, S-J., 2021. Bacteria and metabolic potential in karst caves revealed by intensive bacterial cultivation and genome assembly. Applied Environmental Microbiology, 87: e02440-20. https://doi.org/10.1128/AEM.02440-20

Uwagi

Opracowanie rekordu ze środków MNiSW, umowa nr POPUL/SP/0154/2024/02 w ramach programu "Społeczna odpowiedzialność nauki II" - moduł: Popularyzacja nauki (2025).