Seasonal Variation in Fungi in Beach Sand in Summertime: Stintino (Italy)
Abstract
:1. Introduction
2. Materials and Methods
Sampling Site and Method
3. Methods and Statistical Analysis
3.1. DNA Extraction and Meta-Barcode Sequencing
3.2. Bioinformatics Analysis
4. Results
4.1. Bacterial and Fungal Taxonomy
4.2. Alpha and Beta Diversity
4.3. Effect of Limiting the Number of Visitors to the Beach
5. Discussion
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Mendes, B.; Nascimento, M.J.; Oliveira, J.S. Preliminary characterisation and proposal of microbiological quality standard of sand beaches. Water Sci. Technol. 1993, 27, 453–456. [Google Scholar] [CrossRef]
- Dabrowa, N.; Landau, J.W.; Newcomer, V.D.; Plunkett, O.A. A survey of tide-washed coastal areas of southern California for fungi potentially pathogenic to man. Mycopathol. Appl. Mycol. 1964, 24, 137–150. [Google Scholar] [CrossRef] [PubMed]
- Kishimoto, R.A.; Baker, G.E. Pathogenic and potentially pathogenic fungi isolated from beach sands and selected soils of Oahu, Hawaii. Mycologia 1969, 61, 537–548. [Google Scholar] [CrossRef]
- Aulicino, F.A.; Volterra, L.; Donati, G. Faecal contamination of shore-line sands. Boll. Soc. It. Biol. 1985, 61, 1469–1475. [Google Scholar]
- Larrondo, J.V.; Calvo, M.A. Fungal density in the sands of the Mediterranean coast beaches. Mycophatologia 1989, 108, 185–193. [Google Scholar] [CrossRef] [PubMed]
- Ghinsberg, R.C.; Bar Dov, L.; Rogol, M.; Sheinberg, Y.; Nitzan, Y. Monitoring of selected bacteria and fungi in sand and seawater along the Tel Aviv coast. Microbios 1994, 77, 29–40. [Google Scholar]
- Papadakis, J.A.; Mavridou, A.; Richardson, S.C.; Lampiri, M.; Marcelou, U. Batherrelated microbial and yeast populations in sand and seawater. Water Res. 1997, 31, 799–804. [Google Scholar] [CrossRef]
- Brandão, J.; Gangneux, J.P.; Arikan-Akdagli, S.; Barac, A.; Bostanaru, A.C.; Brito, S.; Bull, M.; Çerikçioğlu, N.; Chapman, B.; Efstratiou, M.A.; et al. Mycosands: Fungal diversity and abundance in beach sand and recreational waters—Relevance to human health. Sci. Total Environ. 2021, 10, 781. [Google Scholar] [CrossRef]
- Steffen, H.C.; Smith, K.; van Deventer, C.; Weiskerger, C.; Bosch, C.; Brandão, J.; Wolfaardt, G.; Botha, A. Health risk posed by direct ingestion of yeasts from polluted river water. Water Res. 2023, 231, 119599. [Google Scholar] [CrossRef]
- Wheeler Alm, E.; Burke, J.; Spain, A. Fecal indicator bacteria are abundant in wet sand at freshwater beaches. Water Res. 2003, 37, 3978–3982. [Google Scholar] [CrossRef] [PubMed]
- Elmanama, A.A.; Fahd, M.I.; Afifi, S.; Abdallah, S.; Bahr, S. Microbiological beach sand quality in Gaza Strip in comparison to seawater quality. Environ. Res. 2005, 99, 1–10. [Google Scholar] [CrossRef]
- Shibata, T.; Solo-Gabriele, H.M. Quantitative Microbial Risk Assessment of Human Illness from Exposure to Marine Beach Sand. Environ. Sci. Technol. 2012, 46, 2799–2805. [Google Scholar] [CrossRef] [PubMed]
- Brandão, J.; Valério, E.; Weiskerger, C.; Veríssimo, C.; Sarioglou, K.; Novak Babič, M.; Solo-Gabriele, H.M.; Sabino, R.; Rebelo, M.T. Strategies for Monitoring Microbial Life in Beach Sand for Protection of Public Health. Int. J. Environ. Res. Public Health 2023, 20, 5710. [Google Scholar] [CrossRef] [PubMed]
- Mancini, L.; D’Angelo, A.M.; Pierdominici, E.; Ferrari, C.; Anselmo, A.; Venturi, L.; Fazzo, L.; Formichetti, P.; Iaconelli, M.; Pennelli, B. Microbiological quality of Italian beach sands. Microchem. J. 2005, 79, 257–261. [Google Scholar] [CrossRef]
- Sato, M.I.Z.; Di Bari, M.; Lamparelli, C.C.; Cristina, T.A.; Coelho, M.C.L.S.; Hachich, E.M. Sanitary quality of sands from marine recreational beaches of São Paulo, Brazil. Braz. J. Microbiol. 2005, 36, 321–326. [Google Scholar] [CrossRef]
- Bonilla, T.D.; Nowosielski, K.; Cuvelier, M.; Hartz, A.; Green, M.; Esiobu, N.; McCorquodale, D.S.; Fleisher, J.M.; Rogerson, A. Prevalence and distribution of fecal indicator organisms in South Florida beach sand and preliminary assessment of health effects associated with beach sand expores. Mar. Pollut. Bull. 2007, 54, 1472–1482. [Google Scholar] [CrossRef] [PubMed]
- Salvo, V.S.; Fabiano, M. Mycological assessment of sediments in Ligurian beaches in the Northwestern Mediterranean: Pathogens and opportunistic pathogens. J. Environ. Manag. 2007, 83, 365–369. [Google Scholar] [CrossRef]
- Vogel, C.; Rogerson, A.; Schatzc, S.; Laubache, H.; Tallman, A.; Fell, J. Prevalence of yeasts in beach sand at three bathing beaches in South Florida. Water Res. 2007, 41, 1915–1920. [Google Scholar] [CrossRef]
- Maciel, N.O.; Johann, S.; Brandão, L.R.; Kucharíková, S.; Morais, C.G.; Oliveira, A.P.; Freitas, G.J.; Borelli, B.M.; Pellizzari, F.M.; Santos, D.A.; et al. Occurrence, antifungal susceptibility, and virulence factors of opportunistic yeasts isolated from Brazilian beaches. Mem. Inst. Oswaldo Cruz 2019, 114, e180566. [Google Scholar] [CrossRef]
- Pereira, E.; Figueira, C.; Aguiar, N.; Vasconcelos, R.; Vasconcelos, S.; Calado, G.; Brandão, J.; Prada, S. Microbiological and mycological beach sand quality in a volcanic environment: Madeira archipelago, Portugal. Sci. Total Environ. 2013, 461–462, 469–479. [Google Scholar] [CrossRef]
- Shah, A.H.; Abdelzaher, A.M.; Phillips, M.; Hernández, R.; Solo-Gabriele, H.M.; Kish, J. Indicator microbes correlate with pathogenic bacteria, yeasts and helminthes in sand at a subtropical recreational beach site. J. Appl. Microbiol. 2011, 110, 1571–1583. [Google Scholar] [CrossRef]
- Sabino, R.; Veríssimo, C.; Cunha, M.A.; Wergikoski, B.; Ferreira, F.C.; Rodrigues, R. Pathogenic fungi: An unacknowledged risk at coast resorts? New insights on microbiological sand quality in Portugal. Mar. Pollut. Bull. 2011, 62, 1506–1511. [Google Scholar] [CrossRef]
- Prüss, A. A review of epidemiological studies from exposure to recreational waters. Int. J. Epidemiol. 1998, 27, 1–9. [Google Scholar] [CrossRef]
- Fattal, B.; Peleg-Olevsky, T.; Agurshy, T.; Shuval, H.I. The association between sea-water pollution as measured by bacterial indicators and morbidity of bathers at Mediterranean beaches in Israel. Chemosphere 1987, 16, 565–570. [Google Scholar] [CrossRef]
- Seyfield, P.L.; Tobin, R.; Brown, N.E.; Ness, P.F. A prospective study of swimming related illness. I: Swimming associated health risk. II Morbidity and the microbiological quality of water. Am. J. Public Health 1985, 9, 1068–1075. [Google Scholar]
- Whitman, R.L.; Przybyla-Kelly, K.; Shively, D.A.; Nevers, M.B.; Byappanahalli, M.N. Hand-mouth transfer and potential for exposure to E. coli and F+ coliphage in beach sand, Chicago, Illinois. J. Water Health 2009, 7, 623–629. [Google Scholar] [CrossRef]
- Heaney, C.D.; Sams, E.; Wing, S.; Marchall, S.; Brenner, K.; Dufour, A.P.; Wade, T.J. Contact with beach sand among beachgoers and risk of illness. Am. J. Epidemiol. 2009, 170, 164–172. [Google Scholar] [CrossRef]
- Dorfman, M.; Rosselot, K.S.; Stoner, N. Testing the Waters: A Guide to Water Quality at Vacation Beaches, 19th ed.; National Resources Defence Council: Washington, DC, USA, 2009. [Google Scholar]
- Fell, J.W. Yeasts in oceanic regions. In Recent Advances in Aquatic Mycology; Jones, E.B.G., Ed.; Elek Science: London, UK, 1976; pp. 93–124. [Google Scholar]
- Fell, J.W.; Ahearn, D.G.; Meyers, S.P.; Roth, F.J., Jr. Isolation of yeasts from Biscayne Bay, Florida and adjacent benthic areas. Limnol. Oceanogr. 1960, 5, 366–371. [Google Scholar] [CrossRef]
- Meyers, S.P.; Ahearn, D.G. Implications of yeasts and yeast-like fungi in marine processes. Veroeff Inst. Meeresforsch. Bremerh 1974, 5, 321–338. [Google Scholar]
- Kohlmeyer, J.; Kohlmeyer, E. Marine Mycology: The Higher Fungi; Academic Press: New York, NY, USA, 1979; p. 690. [Google Scholar]
- Frac, M.; Hannula, S.E.; Belka, M.; Jȩdryczka, M. Fungal biodiversity and their role in soil health. Front. Microbiol. 2018, 9, 707. [Google Scholar] [CrossRef] [PubMed]
- Segata, N.; Izard, J.; Waldron, L.; Gevers, D.; Miropolsky, L.; Garrett, W.S.; Huttenhower, C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 24, R60. [Google Scholar] [CrossRef]
- Adamczyk, K.; Garncarczyk, A.; Antończak, P.; Wcisło-Dziadecka, D. The foot microbiome. J. Cosmet. Dermatol. 2020, 19, 1039–1043. [Google Scholar] [CrossRef] [PubMed]
- Anderson, J.H. In vitro survival of human pathogenic fungi in seawater. Sabouraudia 1979, 7, 1–12. [Google Scholar]
- Samarasinghe, H.; Lu, Y.; Aljohani, R.; Al-Amad, A.; Yoell, H.; Xu, J. Global patterns in culturable soil yeast diversity. iScience 2021, 24, 103098. [Google Scholar] [CrossRef] [PubMed]
- Amend, A. From dandruff to deep-sea vents: Malassezia-like fungi are ecologically hyper-diverse. PLoS Pathog. 2014, 10, e1004277. [Google Scholar] [CrossRef] [PubMed]
- Lai, X.; Cao, L.; Tan, H.; Fang, S.; Huang, Y. Fungal communities from methane hydrate-bearing deep-sea marine sediments in South China Sea. ISME J. 2007, 1, 756–762. [Google Scholar] [CrossRef]
- Le Calvez, T.; Burgaud, G.; Mahe, S.; Barbier, G.; Vandenkoornhuyse, P. Fungal diversity in deep-sea hydrothermal ecosystems. Appl. Environ. Microbiol. 2009, 75, 6415–6421. [Google Scholar] [CrossRef]
- O’Rorke, R.; Lavery, S.D.; Wangm, M.; Nodder, S.D.; Jeffs, A.G. Determining the diet of larvae of the red rock lobster (Jasus edwardsii) using high-throughput DNA sequencing techniques. Mar. Biol. 2013, 161, 551–563. [Google Scholar] [CrossRef]
- Terahara, T.; Chow, S.; Kurogi, H.; Lee, S.H.; Tsukamoto, K. Efficiency of peptide nucleic acid-directed PCR clamping and Its application in the investigation of natural diets of thejapanese eel Leptocephali. PLoS ONE 2011, 6, e25715. [Google Scholar] [CrossRef]
- Arenz, B.E.; Held, B.W.; Jurgens, J.A.; Farrell, R.L.; Blanchette, R.A. Fungal diversity in soils and historic wood from the Ross Sea Region of Antarctica. Soil. Biol. Biochem. 2006, 38, 3057–3064. [Google Scholar] [CrossRef]
- Renker, C.; Alphei, J.; Buscot, F. Soil nematodes associated with the mammal pathogenic fungal genus Malassezia (Basidiomycota: Ustilaginomycetes) in Central European forests. Biol. Fertil. Soils 2003, 37, 70–72. [Google Scholar] [CrossRef]
- Roy, M.; Watthana, S.; Stier, A.; Richard, F.; Vessabutr, S. Two mycoheterotrophic orchids from Thailand tropical dipterocarpacean forests associate with a broad diversity of ectomycorrhizal fungi. BMC Biol. 2009, 7, 51. [Google Scholar] [CrossRef] [PubMed]
- Pitkaranta, M.; Meklin, T.; Hyvarinen, A.; Paulin, L.; Auvinen, P. Analysis of fungal flora in indoor dust by ribosomal DNA sequence analysis, quantitative PCR, and culture. Appl. Environ. Microbiol. 2007, 74, 233–244. [Google Scholar] [CrossRef] [PubMed]
- Dinulos, J.G. Habif’s Clinical Dermatology. Elsevier Health Sciences: Amsterdam, The Netherlands, 2019. [Google Scholar]
- Matallah-Boutiba, A.; Benmessaoud, N.; Messaoui, N.; Boutiba, Z. Microbiological Sandy Beach Quality in Western Algeria. J. Mar. Biol. Ocean. Oceanogr. 2017, 6, 1. [Google Scholar]
- Salleh, S.L. Microfungal community in sandy beaches located in Kedah, Pahang and Sabah, Malaysia. Stud. Fungi 2018, 6, 321–332. [Google Scholar] [CrossRef]
- Madhanraj, P.; Manorajan, S.; Nadimuthu, N.; Panneerselvam, A. An investigation of the mycoflora in the sand dune soils of Tamilnadu coast, India. Adv. Appl. Sci. Res. 2010, 1, 160–167. [Google Scholar]
- Vidal, P.; Sanchez-Puelles, J.M.; Milan, D.; Guarro, J. Chrysosporium on the west coast of Sweden. Acta Dermatol. Venereol. 1966, 46, 78–81. [Google Scholar]
- Müller, G. Occurrence of dermatophytes in the sands of European beaches. Sci. Total Environ. 1973, 2, 116–118. [Google Scholar] [CrossRef]
- Sousa, M.L.R. Mycoses; National Institute of Health (INSA), Centre of Epidemiologic Surveillance of Transmissible Diseases (Epidemiology Bulletin No. 5): Lisbon, Portugal, 1990. [Google Scholar]
- Ulfig, K.; Guarro, J.; Cano, J.; Gene, J.; Vidal, P.; Figueras, M.J. General assessment of the occurrence of keratinolytic fungi in river and marine beach sediments of Catalonian waters (Spain). Water Air Soil Pollut. 1997, 94, 275–287. [Google Scholar] [CrossRef]
- Londono, C.O.; Fernandez, R.R.; Gulloso, E.R.M. Dermatophytes in the coastal area of district of Riohacha, La Guajira. Contemp. Eng. Sci. 2018, 11, 4691–4699. [Google Scholar] [CrossRef]
- Zhan, P.; Liu, W. The changing face of dermatophytic infections worldwide. Mycopathologia 2017, 182, 77–86. [Google Scholar] [CrossRef] [PubMed]
- Trofa, D.; Gácser, A.; Nosanchuk, J.D. Candida parapsilosis, an emerging fungal pathogen. Clin. Microbiol. Rev. 2008, 21, 606–625. [Google Scholar] [CrossRef] [PubMed]
- Colombo, A.L.; Nucci, M.; Park, B.J.; Nouer, S.A.; Arthington-Skaggs, B.; da Matta, D.A. Epidemiology of candidemia in Brazil: A nationwide sentinel surveillance of candidemia in eleven medical centers. J. Clin. Microbiol. 2006, 44, 2816–28123. [Google Scholar] [CrossRef] [PubMed]
- Fernández-Ruiz, M.; Guinea, J.; Puig-Asensio, M.; Zaragoza, Ó.; Almirante, B.; Cuenca-Estrella, M. Fungemia due to rare opportunistic yeasts: Data from a population-based surveillance in Spain. Med. Mycol. 2017, 55, 125–136. [Google Scholar] [CrossRef]
- Pitt, J.I. The current role of Aspergillus and Penicillium in human and animal health. J. Med. Vet. Mycol. 1994, 32, 17–32. [Google Scholar] [CrossRef]
- Vitte, J.; Michel, M.; Malinovschi, A.; Caminati, M.; Odebode, A.; Annesi-Maesano, I.; Caimmi, D.P.; Cassagne, C.; Demoly, P.; Heffler, E.; et al. EAACI Task Force on Allergic Bronchopulmonary Aspergillosis. Fungal exposome, human health, and unmet needs: A 2022 update with special focus on allergy. Allergy 2022, 77, 3199–3216. [Google Scholar] [CrossRef]
Summer | Winter | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Species | Localization (Skin) | C 2016/18 | C 2019/20 | R 2016/18 | R 2019/20 | D 2016/18 | D 2019/20 | C 2016/18 | C 2019/20 | R 2016/18 | R 2019/20 | D 2016/18 | D 2019/20 |
Candida parapsilosis | Foot | 18.8% | 0.10% | 0.42% | |||||||||
Candida tropicalis | Nails | 1.33% | 0.01% | ||||||||||
Candida orthopsilosis | Newborn skin | 0.80% | |||||||||||
Candida albicans | Foot | 0.14% | 0.02% | ||||||||||
Candida boidinii | Back | 0.04% | |||||||||||
Saccharomyces cerevisiae | Foot | 0.39% | 0.26% | 0.03% | |||||||||
Rhodotorula mucilaginosa | Foot | 0.14% | 0.16% | 0.01% | 0.01% | 0.02% | 0.08% | ||||||
Malassezia restricta | Foot, back | 0.32% | 0.03% | 0.02% | 0.09% | 0.09% | 0.04% | 0.01% | 0.04% | 0.01% | |||
Malassezia arunalokei | Seborrheic zone | 0.04% | |||||||||||
Malassezia globosa | Back | 0.03% | 0.02% | ||||||||||
Aspergillus penicillioides | Head (sebum) | 0.48% | 5.05% | ||||||||||
Fungi of probable human origin: | 22.51% | 5.64% | 0.45% | 0.12% | 0.01% | 0.11% | 0.08% | 0.04% | 0.01% | 0.04% | 0.01% | ||
Candida | 21.1% | 0.13% | 0.42% | ||||||||||
Malassezia | 0.40% | 0.05% | 0.02% | 0.09% | 0.09% | 0.04% | 0.01% | 0.04% | 0.01% | ||||
Other yeasts | 0.53% | ||||||||||||
Molds | 0.48% | 5.05% |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Deligios, M.; Mazzarello, V.; Fiamma, M.; Barac, A.; Diana, L.; Ferrari, M.; Murgia, M.; Paglietti, B.; Rubino, S. Seasonal Variation in Fungi in Beach Sand in Summertime: Stintino (Italy). Int. J. Environ. Res. Public Health 2023, 20, 7134. https://doi.org/10.3390/ijerph20237134
Deligios M, Mazzarello V, Fiamma M, Barac A, Diana L, Ferrari M, Murgia M, Paglietti B, Rubino S. Seasonal Variation in Fungi in Beach Sand in Summertime: Stintino (Italy). International Journal of Environmental Research and Public Health. 2023; 20(23):7134. https://doi.org/10.3390/ijerph20237134
Chicago/Turabian StyleDeligios, Massimo, Vittorio Mazzarello, Maura Fiamma, Aleksandra Barac, Lorenzo Diana, Marco Ferrari, Manuela Murgia, Bianca Paglietti, and Salvatore Rubino. 2023. "Seasonal Variation in Fungi in Beach Sand in Summertime: Stintino (Italy)" International Journal of Environmental Research and Public Health 20, no. 23: 7134. https://doi.org/10.3390/ijerph20237134