The fungal community associated with beach sand and plants located along marine coasts are an under-studied area of research despite its potential relevance to human health. In this study, we isolated and identified the cultivable mycobiota associated with sand and plants collected along the coast of Gran Canaria (Spain) using culture-dependent and -independent methods. Clinically relevant species belonging to Cryptococcus spp. and related genera such as Naganishia and Papilotrema were isolated and identified from shoreline plants. Moreover, Candidatropicalis was isolated from beach sand, and Aspergillus fumigatus and Aspergillus terreus strains were associated with both types of samples (i.e., plants and beach sand). We conclude that beach sand and shoreline plants are potential reservoirs of fungi of high clinical interest. We recommend including beach sand and plants from the environment when assessing the quality of marine coastal systems. Our results open a framework for studying the natural marine environment and its role in the epidemiology of infectious diseases in order to more accurately manage public health.
References
[1]
Biedunkiewicz, A., Sucharzewska, E., Kulesza, K., Nowacka, K. and Kubiak, D. (2019) Phyllosphere of Submerged Plants in Bathing Lakes as a Reservoir of Fungi—Potential Human Pathogens. Microbial Ecology, 79, 552-561. https://doi.org/10.1007/s00248-019-01447-y
[2]
Akinbobola, A.B., Kean, R., Hanifi, S.M.A. and Quilliam, R.S. (2023) Environmental Reservoirs of the Drug-Resistant Pathogenic Yeast Candida auris. PLOS Pathogens, 19, e1011268. https://doi.org/10.1371/journal.ppat.1011268
[3]
Bonifaz, A., García-Salazar, E. and Frías-De-León, M.G. (2024) Climate Change Exacerbating Fungal Disease Disparities. Current Fungal Infection Reports, 18, 1-12. https://doi.org/10.1007/s12281-023-00479-9
[4]
Gangneux, J.-P., Brandao, J., Segal, E., Arikan-Akdagli, S., Barac, A., Bertout, S., et al. (2024) Knowledge and Regulation on Fungal Contamination of Sand and Water: Progress Report and Perspectives. Medical Mycology, 62, Article myad137. https://doi.org/10.1093/mmy/myad137
[5]
Magoye, E., Nägeli, L., Bühlmann, A., Hilber-Bodmer, M., Keller, P., Mühlethaler, K., et al. (2023) Clinical Aureobasidium Isolates Are More Fungicide Sensitive than Many Agricultural Isolates. Microbiology Spectrum, 11, e05299-22. https://doi.org/10.1128/spectrum.05299-22
[6]
Dietl, A.-M., Vahedi-Shahandashti, R., Kandelbauer, C., Kraak, B., Lackner, M., Houbraken, J., et al. (2021) The Environmental Spread of Aspergillus terreus in Tyrol, Austria. Microorganisms, 9, Article 539. https://doi.org/10.3390/microorganisms9030539
[7]
Liu, F., Zeng, M., Zhou, X., Huang, F. and Song, Z. (2024) Aspergillus fumigatus Escape Mechanisms from Its Harsh Survival Environments. Applied Microbiology and Biotechnology, 108, Article No. 53. https://doi.org/10.1007/s00253-023-12952-z
[8]
Nouraei, H., Gharechahi, F., Zareshahrabadi, Z., Zomorodian, K., Gharavi, A., Khodadadi, H., Ansari, S., Amirzadeh, N. and Pakshir, K. (2024) Molecular Characterization of Non-Cryptococcus Yeasts Communities Isolated from Eucalyptus Trees. Current Medical Mycology, 10, e2024.345184.1500.
[9]
Vogel, C., Rogerson, A., Schatz, S., Laubach, H., Tallman, A. and Fell, J. (2007) Prevalence of Yeasts in Beach Sand at Three Bathing Beaches in South Florida. Water Research, 41, 1915-1920. https://doi.org/10.1016/j.watres.2007.02.010
[10]
Arora, P., Singh, P., Wang, Y., Yadav, A., Pawar, K., Singh, A., et al. (2021) Environmental Isolation of Candida auris from the Coastal Wetlands of Andaman Islands, India. mBio, 12, e03181-20. https://doi.org/10.1128/mbio.03181-20
[11]
Mitchell, T.G., Castañeda, E., Nielsen, K., Wanke, B. and Lazéra, M.S. (2010) Environmental Niches for Cryptococcus neoformans and Cryptococcus gattii. In: Heitman, J., Kozel, T.R., Kyung, J., Kwon-Chung, J.R. and Perfect, A.C., Ed., Cryptococcus: From Human Pathogen to Model Yeast, American Society for Microbiology Press, 235-259. https://doi.org/10.1128/9781555816858.ch18
[12]
Cirer Costa, J.C. (2023) Creation of Mass Sun-and-Beach Tourism in Spain: The Definition of the Tourist Product through Architecture. Journal of Historical Research in Marketing, 16, 71-95. https://doi.org/10.1108/jhrm-06-2023-0020
[13]
Domsch, K.H., Gams, W. and Anderson, T.H. (1980) Compendium of Soil Fungi. Academic Press.
[14]
Von Arx, J.A. (1981) The Genera of Fungi Sporulating in Pure Culture. Cramer.
[15]
Kiffer, E. and Morelet, M. (1997) Les Deuteromycetes: Classification et cles d’Identification Generique. INRA Editions.
[16]
Walsh, T.J., Hayden, R.T. and Larone, D.H. (2018) Larone’s Medically Important Fungi: A Guide to Identification. American Society for Microbiology. https://doi.org/10.1128/9781555819880
[17]
Kidd, S., Halliday, C. and Ellis, D. (2022) Descriptions of Medical Fungi. CABI. https://doi.org/10.1079/9781800622340.0000
[18]
Murray, M.G. and Thompson, W.F. (1980) Rapid Isolation of High Molecular Weight Plant DNA. Nucleic Acids Research, 8, 4321-4326. https://doi.org/10.1093/nar/8.19.4321
[19]
Garcia-Jimenez, P., Carrasco-Acosta, M., Payá, C.E., López, I.A., Rodríguez, J.R.B. and Melián, J.A.H. (2019) Composition and Molecular Identification of Bacterial Community in Seawater Desalination Plants. Advances in Microbiology, 9, 863-876. https://doi.org/10.4236/aim.2019.910053
[20]
Glass, N.L. and Donaldson, G.C. (1995) Development of Primer Sets Designed for Use with the PCR to Amplify Conserved Genes from Filamentous Ascomycetes. Applied and Environmental Microbiology, 61, 1323-1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
[21]
Peterson, S.W. and Sigler, L. (2002) Four New Penicillium Species Having Thysanophora-Like Melanized Conidiophores. Mycological Research, 106, 1109-1118. https://doi.org/10.1017/s0953756202006433
[22]
Kurtzman, C.P. and Robnett, C.J. (1997) Identification of Clinically Important Ascomycetous Yeasts Based on Nucleotide Divergence in the 5’ End of the Large-Subunit (26S) Ribosomal DNA Gene. Journal of Clinical Microbiology, 35, 1216-1223. https://doi.org/10.1128/jcm.35.5.1216-1223.1997
[23]
White, T.J., Bruns, T., Lee, S. and Taylor, J. (1990) Amplifcation and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T.J., Eds., PCR Protocols: A Guide Methods Applications, Academic Press, 315-322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
[24]
Oliveros, J.C. (2024) Venny. An Interactive Tool for Comparing Lists with Venn’s Diagrams. https://bioinfogp.cnb.csic.es/tools/venny/
[25]
Raghukumar, S. (2017) Fungi in Coastal and Oceanic Marine Ecosystems: Marine Fungi. Springer. https://doi.org/10.1007/978-3-319-54304-8
[26]
Li, S., Hartman, G.L., Jarvis, B.B. and Tak, H. (2002) A Stachybotryschartarum Isolate from Soybean. Mycopathologia, 154, 41-49. https://doi.org/10.1023/A:1015297907991
[27]
Bhansali, R.R. (2011) Ganoderma Diseases of Woody Plants of Indian Arid Zone and Their Biological Control. In: Michel Mérillon, J. and Gopal Ramawat, K., Eds., Plant Defence: Biological Control,Springer, 209-239.
[28]
Hurtado, J.C., Castillo, P., Fernandes, F., Navarro, M., Lovane, L., Casas, I., et al. (2019) Mortality Due to Cryptococcus neoformans and Cryptococcus gattii in Low-Income Settings: An Autopsy Study. Scientific Reports, 9, Article No. 7493. https://doi.org/10.1038/s41598-019-43941-w
[29]
Springer, D.J., Mohan, R. and Heitman, J. (2017) Plants Promote Mating and Dispersal of the Human Pathogenic Fungus Cryptococcus. PLOS ONE, 12, e0171695. https://doi.org/10.1371/journal.pone.0171695
[30]
de Souza Oliveira, L.S., Pinto, L.M., de Medeiros, M.A.P., Toffaletti, D.L., Tenor, J.L., Barros, T.F., et al. (2021) Comparison of Cryptococcus Gattii/neoformans Species Complex to Related Genera (Papiliotrema and Naganishia) Reveal Variances in Virulence Associated Factors and Antifungal Susceptibility. Frontiers in Cellular and Infection Microbiology, 11, Article 642658. https://doi.org/10.3389/fcimb.2021.642658
[31]
Zhang, S., Wang, L., Han, Q., Sun, A., Liu, X. and Xue, L. (2022) Lung Cancer Coexisting with Papiliotrema flavescens Infection Diagnosed by Next-Generation Sequencing: A Case Report. BMC Infectious Diseases, 22, Article No. 684. https://doi.org/10.1186/s12879-022-07591-0
[32]
Aghaei Gharehbolagh, S., Nasimi, M., Agha Kuchak Afshari, S., Ghasemi, Z. and Rezaie, S. (2017) First Case of Superficial Infection Due to Naganishia albida (Formerly Cryptococcus albidus) in Iran: A Review of the Literature. Current Medical Mycology, 3, 33-37. https://doi.org/10.29252/cmm.3.2.33
[33]
Pakshir, K., Fakhim, H., Vaezi, A., Meis, J.F., Mahmoodi, M., Zomorodian, K., et al. (2018) Molecular Epidemiology of Environmental Cryptococcus Species Isolates Based on Amplified Fragment Length Polymorphism. Journal de Mycologie Médicale, 28, 599-605. https://doi.org/10.1016/j.mycmed.2018.09.005
[34]
Alami, S., Sekkal, I., Aoufi, S., Lyagoubi, M., Benzekri, L. and Senouci, K. (2022) Subcutaneous Phaeohyphomycosis Caused by Aureobasidium pullulans in an Immunocompetent Carpenter. Medical Mycology Case Reports, 36, 1-4. https://doi.org/10.1016/j.mmcr.2022.02.003
[35]
Mikulska, M., Furfaro, E., Dettori, S., Giacobbe, D.R., Magnasco, L., Dentone, C., et al. (2022) Aspergillus-PCR in Bronchoalveolar Lavage-Diagnostic Accuracy for Invasive Pulmonary Aspergillosis in Critically Ill Patients. Mycoses, 65, 411-418. https://doi.org/10.1111/myc.13428
