Fungal Diversity in Marmaris Public Beach Sand (Turkey)

doi:10.21203/rs.3.rs-1605405/v1

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Fungal Diversity in Marmaris Public Beach Sand (Turkey)

https://doi.org/10.21203/rs.3.rs-1605405/v1

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In this study, which was carried out to determine the fungal diversity in the sand of Marmaris public beach, a total of 30 sand samples were taken, 5 from dry and 5 wet regions, in June, July and August when the public beach is used extensively. Soil dilution method was used to isolate fungi from sand samples. Inoculation was made by transferring 1 ml of 10^− 4 dilutions to petri dishes containing Rosebengal Chloramphenicol Agar. As a result of the isolation and identification processes, 22 fungal species belonging to the genera Aspergillus, Beauveria, Cladosporium, Drechslera, Fusarium, Humicola, Penicillium, Phoma, Scopulariopsis, Stachybotrys and Trichophyton were obtained. Qualitatively and quantitatively Aspergillus genus was found to be dominant among the fungal genera, and Aspergillus nidulans was found to be dominant among the fungi species. According to the results of the research, it was determined that dry beach sand contains more fungi than wet beach sand. The isolation of fungi that cause various infections and mycotoxicosis in humans, such as Aspergillus, Fusarium, Phoma, Scopulariopsis, Stachybotrys and Trichophyton, from beach sand shows the necessity of keeping the beaches under control and following general hygiene rules in terms of community and environmental health. In addition, it was concluded that many studies should be conducted to understand the risks on public health of fungi found in beach sands, to ensure public safety and to determine the level of contamination.

Fungal contamination

Microfungi

Beach sand

Marmaris public beach

Beach sand is a habitat that hosts a variety of pathogenic or non-pathogenic microorganisms called microsammon. Some of the microorganisms are native members (autochthonous) adapted to that environment, and some of them are variable members (allochthonous) that are transported by some factors (human, animal, atmospheric movements, precipitation, wastewater contamination). The physical, chemical and biological properties of beach sand can also be effective on the diversity of microorganisms (WHO 2003; Mancini et al. 2005; Zakaria et al. 2011; Pereira et al. 2013; Whitman et al. 2014; Romao et al. 2015; Abreu et al. 2016; Solo-Gabriele et al. 2016; Samarasekera and Abeygunawardena 2017; Testolin et al. 2017). In addition to these, many environmental factors including abiotic factors such as humidity, temperature, sunlight, nutrients and biotic factors such as competition and predation affect the microbial community in beach sand (Whitman et al. 2014).

Fungi constitute a significant part of the microsammon found in the beach sand. Fungi are widely distributed in nature and their spores are easily spread to the environment by air and water (Romao et al. 2015). Fungi can be divided into three main groups according to their potential human pathogenesis: primary pathogens that can develop by invading the tissues of a healthy host, opportunistic pathogens that are usually saprophytes and cause infection in immunocompromised individuals, and dermatophytes that invade the host and infiltrate keratinic tissues (Mancini et al. 2005).

People are exposed to autochthonous and allochthonous microorganisms found in the sand during their activities on the beach. Although most of these microorganisms, which emerge when beach sands are heavily contaminated with human and animal wastes, are harmless, some of them may show pathogenic and potentially pathogenic properties and cause infections in beach residents (Mancini et al. 2005; Zakaria et al. 2011; Whitman et al. 2014; Abreu et al. 2016; Solo-Gabriele et al. 2016; Samarasekera and Abeygunawardena 2017; Testolin et al. 2017).

Beaches are popular places for activities such as swimming, entertainment and sports, and are preferred by local and foreign tourists. For this reason, studies that define fungal diversity and the risks of disease transmission in beach sands will be of great benefit in terms of public health. In connection with this, studies on microsammon in beach sands have been increasing in recent years. Italy (Mancini et al. 2005), Portugal (Pereira et al. 2013; Abreu et al. 2016; Sabino et al. 2011), Brazil (Testolin et al. 2017; Viera et al. 2001; Gomes et al. 2008), Mexico (Gonzalez et al. 2000), Egypt (Migahed 2003), Palestine (Abdallah et al. 2005), United Arab Emirates (Al Marzooqi and Al Anouti 2014), Sri Lanka (Samarasekera and Abeygunawardena 2017), Malaysia (Zakaria et al. 2011) and Morocco (Abdallaoui et al. 2007) have been researched on the subject, but no study has been found in Turkey that determines the fungi found in beach sands at the genus and species level.

A large number of studies are required to understand the risks of fungi in beach sands in terms of public health, to ensure public safety and to determine the level of contamination in beach sands. This issue is of great importance especially for the touristic coastal cities of Turkey. The determination of fungal diversity in beach sands will both help control those that are important for human health and increase awareness on the subject. Marmaris is one of the important tourism cities of Turkey and the world, and is flooded by local and foreign visitors during the summer season. The public beach in the city center is heavily used by visitors especially in June, July and August. For this reason, there are risks of infection, transmission and transportation. This study, which emerged in the light of the information mentioned above, aims to determine the fungal diversity in the sand of Marmaris Public Beach.

In this study, which was carried out to determine the fungal diversity in the sand of Marmaris Public Beach, a total of 30 sand samples were taken, 5 from dry and 5 wet areas, in June, July and August when the public beach is used extensively. Sampling was made by taking approximately 200 g of sand with a small sterile shovel from a depth of 10 cm from the surface. Sand samples were brought to the laboratory in sterile polyethylene bags and processed for fungal isolation. Those waiting in line for processing were kept in the refrigerator. In addition, for some physical and chemical analyzes of beach sand, 2 kg sand samples were taken separately from the dry and wet regions in larger polyethylene bags and brought to Muğla Sıtkı Koçman University Muğla Agricultural Purpose Soil, Plant and Irrigation Water Analysis Laboratory.

"Soil Dilution Method" was used to isolate fungi from sand samples. From the dilution series prepared according to this method, from the bottle diluted at a ratio of 10^− 4, 1 ml was poured into petri dishes containing Rosebengal Chloramphenicol Agar (Merck) medium with sterile pipette (Özkan and Gür 2000; Göçmen and Özkan 2001). The cultivated petri dishes were incubated at 27⁰C for two weeks. Developing fungal colonies were counted, Penicillium and Aspergillus fungi were transferred to petri dishes containing Czapek Dox Agar (CzDA, Modified, Oxoid), others Malt Extract Agar (MEA, Merck) for diagnostic purposes and incubated at 27⁰C for two weeks. The fungi obtained after the incubation period were identified as a result of macroscopic (cultural characteristics) and microscopic examinations made by considering the relevant references (Domsch et al. 1980; Hasenekoğlu 1991; Ellis et al. 2007; Refai and El-Yazid 2014).

Some properties of the beach sand, where the dry region has a sandy texture and the wet region has a sandy loam texture, are given in Table 1. Looking at Table 1, it is seen that the beach sand is slightly alkaline, the amount of organic matter is low, the amount of lime is low, the dry region has no salt and the wet region has low salty features.

Table 1

Some features of Marmaris public beach sand
Beach sand	Texture	% Humidity	pH	Salinity	Organic matter	Lime
Dry	Sandy	2.04	8.33	0.19	0.37	2.45
Wet	Sandy loam	42.25	8.25	5.65	1.29	4.68

Table 1 Some features of Marmaris public beach sand

As a result of the fungal analysis of the beach sand, 22 different fungi species belonging to the genera Aspergillus, Beauveria, Cladosporium, Drechslera, Fusarium, Humicola, Penicillium, Phoma, Scopulariopsis, Stachybotrys and Trichophyton were obtained. Aspergillus genus was found to be dominant (68%) in terms of both colony number and species richness (Table 2). Among the fungal species, Aspergillus nidulans was obtained with a higher frequency (21.34%) compared to the others (Table 3). Domsch et al. (1980) and Hasenekoğlu (1991) state that Aspergillus species are commonly found in warm climate soils. Our findings are in agreement with these views. Indeed, Migahed (2003) Egypt, Mancini et al. (2005) Italy, Abdallaoui et al. (2007) Fas, Gomes et al. (2008) Brazil, Zakaria et al. (2011) Malaysia, Pereira et al. (2013) Portugal, Al Marzooqi and Al Anouti (2014) Abu Dhabi found fungi of the genus Aspergillus widely in their studies on beach sands.

Table 2

Distributions of microfungal genera in the Marmaris Public Beach Sand
Microfungal genera	Colony numbers	Ratio to total colony number (%)
Microfungal genera	Dry Weight sand sand Total	Ratio to total colony number (%)
Aspergillus	49 2 51	68.00
Beauveria	2 - 2	2.67
Cladosporium	5 4 9	12.00
Drechslera	1 - 1	1.33
Fusarium	1 - 1	1.33
Humicola	1 - 1	1.33
Penicillium	3 - 3	4.00
Phoma sp.	1 - 1	1.33
Scopulariopsis	2 - 2	2.67
Stachybotrys	2 - 2	2.67
Trichophyton	2 - 2	2.67
Total colony numbers	69 6 75	100

Table 3

Distributions of microfungal species in the Marmaris Public Beach Sand
Microfungal species	Colony numbers			Ratio to total colony number (%)
Microfungal species	Dry sand	Weight sand	Total	Ratio to total colony number (%)
Aspergillus candidus Link ex Link	6	-	6	8
Aspergillus flavipes (Bain. & Sart.) Thom & Church	6	-	6	8
Aspergillus flavus Link ex Gray	2	-	2	2.67
Aspergillus fumigatus Fresen.	8	1	9	12
Aspergillus nidulans (Eidam) Winter	15	1	16	21.34
Aspergillus niveus Bolchwitz	1	-	1	1.33
Aspergillus ochraceus Wilhelm	1	-	1	1.33
Aspergillus oryzae (Ahlburg) Cohn	8	-	8	10.67
Aspergillus terreus Thom	1	-	1	1.33
Aspergillus wentii Wehmer	1	-	1	1.33
Beauveria alba (Limber) Saccas	2	-	2	2.67
Cladosporium cladosporioides (Fr.) Vries	3	4	7	9.33
Cladosporium herbarum (Pers.) Link	2	-	2	2.67
Drechslera biseptata (Sacc.&Roum.) Richardson & Fraser	1	-	1	1.33
Fusarium moniliforme Sheld.	1	-	1	1.33
Humicola grisea Traaen var. grisea	1	-	1	1.33
Penicillium chrysogenum Thom	2	-	2	2.67
Penicillium variabile Sopp	1	-	1	1.33
Phoma sp. Sacc.	1	-	1	1.33
Scopulariopsis koningii (Oudem.) Vuill.	2	-	2	2.67
Stachybotrys chartarum (Ehrenb. ex Link) Hughes	2	-	2	2.67
Trichophyton verrucosum Bodin	2	-	2	2.67
Total colony numbers	69	6	75	100

In this study, a total of 69 fungal colonies (cfu) were obtained on dry beach sand and 6 fungal colonies (cfu) on wet beach sand (Tables 2 and 3). Considering the amount of colony forming units (cfu), it is seen that the number of fungi is low. This was an expected outcome. Because, the effect of sun rays, low amount of organic matter, the slightly alkaline pH value and the sandy texture suggest that are on the number of fungi have a reducing effect. As a matter of fact, some researchers (Gonzalea et al. 2000; Migahed 2003; Gomes et al. 2008; Sabino et al. 2011; Zakaria et al. 2011; Al Marzooqi and Al Anouti 2014; Whitman et al. 2014; Testolin et al. 2017) state that factors such as organic matter amount, pH value, water content, the texture of the beach sand, nutrient element, and sun rays are effective.

Table 2 Distributions of microfungal genera in the Marmaris Public Beach Sand

Table 3 Distributions of microfungal species in the Marmaris Public Beach Sand

When Tables 2 and 3 are examined, it is understood that the dry region contains more fungi qualitatively and quantitatively than the wet region. Sabino et al. (2011) and Vieira et al. (2001) obtained more fungi in dry beach sand in their study. Our findings agree with these references.

Fungi belonging to the genus Aspergillus generally appear in warm climate soils, compost, decaying plant parts, and stored grains (Domsch et al. 1980; Hasenekoğlu 1991). A. candidus is widely distributed in tropical and subtropical regions. It is reported that it is isolated from neutral and alkaline, sandy, salty soils and desert soils (Domsch et al. 1980). In this study, 6 colonies were obtained from dry beach sand, which has a slightly alkaline and sandy texture (Table 3). A case of onychomycosis related to the effect of A. candidus on human health has been reported (Ahmadi et al. 2012), and it has also been reported to cause respiratory system diseases, invasive aspergillosis and otomycosis (Refai and El-Yazid 2014).

Aspergillus flavipes (teleomorph: Fennellia flavipes) is distributed worldwide, especially in tropical, subtropical and Mediterranean regions and is frequently isolated from the soil. It has been reported by Domsch et al. (1980) that it is isolated from sandy soils and salt flats, can be found in neutral or strongly alkaline soils, and can tolerate high soil temperatures. In this study, 6 colonies were isolated from dry beach sand with slightly alkaline and sandy texture (Table 3). No information was found about the infection or disease formation of Aspergillus flavipes in humans.

Aspergillus flavus has a widespread distribution in the world and is mostly found in tropical and subtropical regions. It is stated that it is isolated from saline soils and littoral regions because it tolerates relatively high salt concentrations, and it is also reported that its distribution in the soil does not depend on a certain pH limit or soil depth, since it has high competitiveness (Domsch et al. 1980). In this research, A. flavus was obtained as 2 colonies from dry beach sand (Table 3). A. flavus, which is known to be pathogenic in humans and animals, also affects human health by producing aflatoxin ((Domsch et al. 1980; Ellis et al. 2007). It can also rarely cause lung infections in humans, and less commonly endocarditis and bladder infections. It has been observed several times in the ear and eye sockets of humans, and the state of skin infection has not been fully determined (Domsch et al. 1980).

Aspergillus fumigatus is a cosmopolitan and thermotolerant fungus that can be found almost everywhere. It has been isolated from coastal and marina habitats, sand masses, beach sands, saline soils and desert soils. It develops in soils with a pH value of 5-8.5, and sporulates by developing in temperate soils warmed by the sun (Domsch et al. 1980). In this study, 8 colonies were isolated from dry beach sand and 1 colony from wet beach sand (Table 3). A. fumigatus, which is one of the important pathogens for humans and animals, can also affect human health by producing toxins ((Domsch et al. 1980; Ellis et al. 2007). It rarely causes acute infection in humans. However, the infection may generalize and pass to the cardiovascular system, urinary system and brain. It has also been found in lung tissues. Although it can cause keratitis in the eye, it is mostly found in the human ear as a secondary colonizer. In skin infections, it is generally considered as a secondary invasive agent (Domsch et al. 1980).

Aspergillus nidulans (teleomorph: Emericella nidulans) is a typical soil fungus with widespread distribution in the world. It is reported that it is obtained from desert soils, beach sand, coastal soils washed by tide, red sandy soils poor in organic matter and alkaline soils (Domsch et al. 1980). In this research, 15 colonies from dry beach sand and 1 colony from wet beach sand were isolated (Table 3). A. nidulans can cause disease in humans and animals (Ellis et al. 2007). It can cause mycetomas such as fibrosarcoma, maduromycetoma and osteophilia. It was also observed together with Trichophyton rubrum in a case of onychomycosis (Domsch et al. 1980).

Aspergillus niveus (teleomorph: Emericella nivea) is a fungus mostly isolated from soil (Domsch et al. 1980). In this study, 1 colony was obtained from dry beach sand (Table 3). No information has been found regarding the effect on human health. It was observed in only one case of pulmonary aspergillosis (Auberger et al. 2008).

Aspergillus ochraceus (synonym: Aspergillus alutaceus) is a fungus that is common in soil and some foods (Domsch et al. 1980) and affects human health by producing ochratoxin (Öksüztepe and Erkan 2016). In this study, 1 colony was isolated from dry beach sand (Table 3).

Aspergillus oryzae has been isolated from cultivated soils, meadows, forest soils, air and dried plant parts. It is reported that it is not pathogenic but has been isolated from brain tissue once (Domsch et al. 1980). In this study, 8 colonies were obtained from dry beach sand (Table 3).

Aspergillus terreus is one of the Aspergillus species widely distributed in soils. It also shows a distinct distribution in tropical and subtropical regions (Domsch et al. 1980). In this study, 1 colony was isolated from dry beach sand. It is stated to be pathogenic in humans and animals (Ellis et al. 2007), it can invade human skin and nails, and can be found as a parasite in the human ear (Domsch et al. 1980).

Aspergillus wentii is a very common species, especially in hot climates. It is stated that it is isolated from desert soils, dry soils, rarely alkaline soils and coastal areas (Domsch et al. 1980). In this research, 1 colony was isolated from dry beach sand (Table 3). No information was found about the effect of A. wentii on human health. However, it has been reported that some isolates produce aflatoxins B1 and B2 (Domsch et al. 1980).

Beauveria species are parasitic on insects. Sometimes they are isolated from clinical laboratories as saprophytic contaminants (Ellis et al. 2007). In this study, Beauveria alba was obtained from dry beach sand in the form of 2 colonies (Table 3).

Pathogenic species in the genus Cladosporium were transferred to the genus Cladophialophora (Ellis et al. 2007; Sandoval-Denis et al. 2015). It has been reported that Cladosporium species are rarely associated with human and animal opportunistic infections (Sandoval-Denis et al. 2015). Cladosporium cladosporioides is one of the most common species of the genus Cladosporium in both soil and plant materials. It is usually isolated from the salty beaches of temperate zones. It maintains its vitality on the dried soil surface during the summer season. It was found in association with Phialophora verrucosa in one case of corneal ulcer. It has also been reported to form a fungal ball in the human lung (Domsch et al. 1980). In this research, a total of 7 colonies were isolated, 3 from dry beach sand and 4 from wet beach sand (Table 3).

Cladosporium herbarum is one of the most common species of the genus Cladosporium, together with C. cladosporioides. It is reported that it spreads from the polar regions to the temperate Mediterranean regions and tropical and subtropical regions. It is stated that it is found in dry desert soils and other very dry region soils and high saline estuarine sediments, and is adapted to high salt concentrations (Domsch et al. 1980). In this study, 2 colonies were obtained from dry beach sand (Table 3).

Pathogenic species in the genus Drechslera have been included in the genera Bipolaris and Exserohilum (Ellis et al. 2007; Refai and El-Yazid 2014). However, Drechslera biseptata has recently been reported in brain abscess (Refai and El-Yazid 2014). Drechslera biseptata was isolated from dry beach sand as 1 colony in this study (Table 3).

Most Fusarium species are soil fungi with a cosmopolitan distribution. They rarely show pathogenicity in humans. However, many species that cause storage caries are important toxin producers (Domsch et al. 1980). Nucci and Anaissie (2007) state that Fusarium species have a broad spectrum of infection in humans. They reported these as superficial infections (keratitis and onychomycosis), locally invasive or widespread infections, allergic diseases (sinusitis) and mycotoxicosis. They state that most of these infections occur especially in immunocompromised patients, and that 12 species, including Fusarium moliniforme, are related. Ajello et al. (1985) report a case of mycetoma in the human foot caused by F. moliniforme. In this study, F. moniliforme was obtained as a colony on dry beach sand (Table 3).

Humicola species are widely distributed in neutral or alkaline soils and are sparsely obtained by dilution technique. H. grisea has been isolated from saline soils, desert soils, and highly saline estuarine sediments (Domsch et al. 1980). There is no information about the effect of H. grisea on human health. Only Burns et al. (2015) reported a case of peritonitis associated with peritoneal dialysis caused by Humicola sp. Humicola grisea var. grisea was isolated as 1 colony from dry beach sand in this study (Table 3).

Penicillium chrysogenum is a soil fungus that produces penicillin and is widely distributed in temperate regions. It has been isolated from saline soils, sand dunes and desert soils (Domsch et al. 1980). It is generally not pathogenic in humans. However, Kantarcıoğlu et al. (2004) reported a case of central nervous system infection related to P. chrysogenum. It has also been stated that it can cause systemic mycosis in immunocompromised hosts, and it was found in a case of lung infection with Pneumocystis jiroveci in a patient with acute myeloid leukemia (Shokouhi et al. 2016). In this study, P. chrysogenum was obtained from dry beach sand in the form of 2 colonies (Table 3).

Penicillium variabile is a soil fungus widely distributed in the world. It has also been reported to be isolated from sand dunes, deserts and coastal areas (Domsch et al. 1980). No information was found regarding its pathogenicity in humans. In this study, 1 colony was isolated from dry beach sand (Table 3).

Phoma species have a wide distribution on earth and are found almost ubiquitously in nature. They are usually plant pathogens and rarely cause infections in humans (Ellis et al. 2007; Refai and El-Yazid 2014). They can cause cutaneous, subcutaneous, corneal or systemic infections in humans (Refai and El-Yazid 2014). In this study, Phoma was obtained from dry beach sand in 1 colony (Table 3).

Most of the Scopulariopsis species are ubiquitous soil fungus. A few species (especially S. brevicaulis) are pathogenic to humans, causing onychomycosis and hyalohyphomycosis (Domsch et al. 1980; Ellis et al. 2007). In addition, Marchisio and Fusconi (2001) reported that S. koningii, as a keratinolytic fungus, causes onychomycosis and some other mycosis. In this study, 2 colonies of S. koningii were isolated from dry beach sand (Table 3).

Stachybotrys chartarum is the most common species of its genus, found mainly in dead plant materials, and spread worldwide (Domsch et al. 1980; Refai and El-Yazid 2014). It is stated that it is found in Mediterranean soils, sand dunes, desert soils, and salty soils and can be easily isolated by dilution technique because it is abundantly sporulated (Domsch et al. 1980). The mycotoxin that it produces can cause mycotoxicosis in humans and animals (Domsch et al. 1980; Refai and El-Yazid 2014). It has also been reported that it can cause hypersensitivity pneumonia, rhinitis, allergies, irritation (in the eyes, mouth, nose and throat), and bleeding in the lungs and nose (Refai and El-Yazid 2014). In this study, 2 colonies were obtained from dry beach sand (Table 3).

Trichophyton spp. are dermatophyte fungi and are the infectious agents in humans named as Tinea pedis, T. unguium, T. corporis, T. cruris and T. capitis (Ellis et al. 2007; Poyraz 2006). T. verrucosum is a zoophilic fungus that is distributed worldwide and causes ringworm disease in cattle. Infections in humans result from direct contact with cattle or infected items and are often highly inflammatory, including the scalp, beard, or areas of the body that are infected (nails, skin) (Ellis et al. 2007). In this study, T. verrucosum was isolated from dry beach sand as 2 colonies (Table 3).

As a result, 22 fungal species belonging to 11 genera were obtained from this study. Among these fungi species, there is no fungus that can seriously endanger human health and cause an epidemic. Aspergillus, Fusarium, Phoma, Scopulariopsis, Stachybotrys and Trichophyton from the obtained fungi can cause mycotoxicosis with various infections in humans. The presence of these fungi in the beach sand shows the necessity of keeping the beaches under control and complying with the general hygiene rules in terms of community and environmental health. Beach sands can be contaminated from animals and infected people, and infection can be transmitted from beach sand to other people. For this reason, studies that define fungal diversity and the risks of transmission of infections in beach sands will be of great benefit for public health. A great deal of research is needed to understand the risks to public health of fungi found in beach sands, to ensure public safety and to determine the level of contamination. Determination of fungal diversity in beach sands will both help control those that are important for human health and increase awareness on the subject.

Acknowledgements Thanks to Muğla Sıtkı Koçman University Muğla Agricultural Soil, Plant and Irrigation Water Analysis Laboratory for performing some physical and chemical analyzes of the beach sand.

Conflict of interest The author declare that they do not have any conflict of interest.

Human and Animal Rights This study does not involve any human or animal testing.

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Fungal Diversity in Marmaris Public Beach Sand (Turkey)

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