III.1. External exposome
Airborne fungal spores and subcellular components originate from different sources, for example, soil, plants, animals, and water. Fungal spores are distributed by physical mechanisms of gravity, wind, water and animals. Airborne particles originating from biological sources (viable and nonviable e.g. bacteria, fungal spores, pollen, mites, dead tissues, and pieces of these materials or their metabolic products including endotoxins and mycotoxins) are called bioaerosols (36). Bioaerosols are ubiquitous; they originate mainly from soil and aquatic, animal, vegetal, and anthropogenic sources, become airborne and may travel long distances in the environment before sedimenting in so-called sinks, or settle, e.g. on indoor surfaces or clothing (25,36,37). The wind dispersal fungal spores, ranging from 1 to 30 µm in size, are major components of bioaerosols, where their release, time of flight, survival, and hence fitness for subsequent growth follow a variety of pathways (37–39).
Culture-independent studies have demonstrated a very high diversity of airborne fungal taxa. As an example, each dust sample taken from the outer surface of hundreds of US homes contained more than 1,000 fungal phylotypes, most of which belonging to taxa not been described at the time of the study (25). However, only Cladosporium ,Toxicladosporium , and Alternaria were found in this study in virtually all samples. These were also dominant taxa in terms of abundance, with Cladosporium spp often amounting to 75% of the whole fungal content of samples and Alternaria spp making up to 50% (25). The results of a questionnaire sent to national and regional networks involved in the European Aeroallergen Network (EAN) and counting fungal spore, have shown that most networks (44.7%) identified five or fewer fungal spore types, and only two networks (12.5%) identified more than 20 fungal spore types. On the other hand, all networks examined Alternaria (16), most of themCladosporium (14) and the third more cited spore wasEpicoccum (10). Other fungal spores where cited (45) in the list, but only by 1 to 6 networks (39). Partly overlapping findings were reported from the European urban areas of Bratislava (Slovakia, temperate continental climate), Thessaloniki (Greece, Mediterranean climate), and Madrid (Spain, warm-temperate subtropical climate). The five top abundant Slovakian fungal spores were Cladosporium, Leptosphaeria, Coprinus, Alternaria, and Ganoderma (40), while their Greek counterparts were Cladosporium, Alternaria, Ustilago,and Ascospores (Aspergillus/Penicillium ) (41).Cladosporium, Alternaria, Eurotium, Epicoccum, Penicillium , andSporobolomyces were detected in more than 90% of samples from Madrid (42). In more arid climate types, such as Karachi (Pakistan) and Kuwait, Cladosporium, Alternaria, Aspergillus, andPenicillium were also found among the top frequent airborne fungal spores, together with Curvularia and Periconia in Karachi (43) and Cryptococcus, Candida, Schizophyllum, Fusarium , and Gleotinia in Kuwait (44). Finally, under tropical climates, airborne fungal spores were dominated by Cladosporium, Leptosphaeria, Coprinus, Aspergillus, and Penicillium in Havana (Cuba) using a culture-independent direct identification method (45) and by Penicillium and Aspergillus in Nigeria using a culture-dependent approach (46).
Under temperate climates, seasonal variations usually increase fungal abundance with higher temperatures and rainfall, such as during summer and fall (42). However, very high temperature values may negatively affect the abundance of airborne fungal spores, as observed in Karachi and Lagos (43,46). Significant interannual variations in rainfall are common and associated with variations in airborne fungal abundance (42,45).
Depending on the considered fungi, spore release may occur preferentially during the daytime, as observed for Alternaria,Cladosporium , Epicoccum, and Exosporium or at night, e.g. Coprinus and Leptosphaeria (40). Particulate air pollution such as PM10 is positively correlated with the fungal spore load (40).
To sum up, the nature and abundance of the dominant fungal spores in the atmosphere exhibit marked variations related to climate (mean annual precipitation and temperature, soil pH, plant diversity, distance to coastal regions), season, time of the day, particulate air pollution, and include Cladosporium and Alternaria as consistently predominant genera, followed by Aspergillus and Penicillium,accompanied by locally important airborne fungi, such as Fusarium, Curvularia, Cryptococcus, and Ustilago .
Indoor exposure is paramount, as most people now spend most of their time indoors (47). Fungi can be transported by dust particles, people, pets, and air ventilation systems into the indoor environment. The relative humidity and moisture content of building materials may also control to a certain level the fungal burden present on indoor materials. Water damage, defined as “a moisture problem caused by various leaks of water” (48), is an essential contributor to indoor mold growth, often related to climatic events (e.g ., floods, storms, rising ocean levels) or poor housing standards, including older homes (23,47,49). Indoors, fungi can colonize virtually any material: walls, windows frames, furniture, carpets, books, wallpapers, and even spacecrafts. Biodeterioration due to fungal colonization poses additional health threats, both direct such as skin contact with fungi growing on documents from archives or libraries, and increased airborne spore and mycotoxin load, and indirect due to the toxicity of biocide treatments (50–52).
The abundance of indoor fungal spores shows geographic and seasonal variations related to exchanges between the outdoor and indoor environments, fungal growth, and meteorological conditions (23). The degree of exposure to indoor molds was estimated at 5-10% under cold-temperate climates, and up to 30% in warmer climates (27). An Environmental Relative Moldiness Index (ERMI) may be used as a quantitative marker of indoor mold exposure (49). The original ERMI, developed in the United States of America, is computed using PCR quantification of 36 common indoor molds, of which 26 are related to water damage and 10 are not (53). In order to acknowledge local fungal variability at the levels of species and abundance, the need for an adapted ERMI was demonstrated (54).
Exposure to mold also occurs at various workplaces. A distinction has to be made between the intentional use of molds and unintentional exposure to moldy materials. The intentional use of molds in workplaces is found in food production, pharmaceutical production and microbiological laboratories. Representatives of the fungal genus Penicillium are found in ripen cheese and salamis and produce antibiotics.Aspergillus niger produces citric acid from residues of the sugar industry. In microbiology laboratories, workers come into contact with molds when growing and multiplying microorganisms. Many more workers come into contact with mold unintentionally: farmers working in fields or keeping animals, waste processors sorting by hand in waste management, wood processors handling moldy wood, metal workers inhaling contaminated cooling lubricants, renovating houses, to name just a few areas.
Despite the diversity of indoor molds, with more than 80 species currently described, and the fact that indoor air may be 70–100 times more contaminated than outdoor air (55,56), there are only four genera of significant importance: Aspergillus, Penicillium, Alternaria , and Cladosporium (47).