Folia Biologica et Oecologica 10: 18–26 (2014) Acta Universitatis Lodziensis

Aeromycology: studies of fungi in aeroplankton

MAŁGORZATA JĘDRYCZKA Institute of Genetics of the Polish Academy of Sciences, Strzeszyńska 34, 60-479 Poznań, Poland E-mail: [email protected]

ABSTRACT

Air is a natural environment for of many genera and species of fungi. Despite its small size and a significant dispersion they have a great impact on human health and different areas of our activities, such as agricultural production. The study on spores of fungi that belong to aeroplankton or bioaerosole is called aeromycology. The most frequent fungi present in the air are Cladosporium and Alternaria species. Their numbers are abundant regardless of latitude and height above the sea level and above the ground. They mostly originate from agricultural environment. Other frequently listed species of fungi, whose spores are present in the air include of Aspergillus, Penicillium, Fusarium, Sclerotinia and Ganoderma. The concentration of spores in the air strongly depends on the abundance of their formation during the studied period. This in turn relates to geobotanical region, vegetation, degree of urbanization, climatic conditions, season, current weather, force and direction, local microclimate, and many other factors. Changes in humidity affect the concentration of different types of fungal spores. In general they are divided to ‘dry’ (Alternaria, Cladosporium, Puccinia, Ustilago, Melampsora, Epicoccum, Drechslera) and ‘wet’ (Didymella, Fusarium, Ganoderma, Gliocladium, Leptosphaeria, Verticillium). Study of the composition of species and genera are being done using different types of samplers, mostly volumetric instruments. Visual identification is based on colony morphology of the and the shape and size of spores. The identification at the species level is possible with molecular tools. Methods based on DNA/RNA amplification are very sensitive and accurate. They allow the identification below the species level, e.g. chemotypes, mating types or isolates with genes or alleles of interest. Aerobiological monitoring is widely used in the epidemiology of human diseases (inhalant allergies) and infections of arable crops (decision support systems for the protection of cultivated ). Aeromycology is interconnected with such diverse areas as industrial , bioterrorism, ecology, climatology or even speleology and cultural heritage.

KEY WORDS: aerobiology, aeromycology, aeroplankton, Alternaria, Cladosporium DOI: 10.2478/fobio-2014-0013 FOLIA BIOLOGICA ET OECOLOGICA

Introduction Air is a natural habitat of numerous or even continents. This phenomenon is fungi, mostly existing there in the form called a long-distance dispersal and it is of spores, their clusters, or – on contrast regarded as an important survival – spore and mycelium fragments. Spores strategy for many organisms. Moving of of some fungal genera are very frequent spores with the air currents allows fungi in air samples, often outnumbering infect new plants of the same host, find grains, on which most of research have new hosts, reach and colonize new focused for many years. Small size and regions or move in between summer and great difficulties to identify the species winter habitats (Brown & Hovmøller based on single spores led to great 2002). Modern agriculture, with greatly underestimation of their presence in the reduced plant and huge . Recent fast development of monocultures increases the risk of global aeromycology, supported with molecular spread of some plant pathogens. Limited tools shows the importance of fungi in genetic variability of modern plant aeroplankton. Fungal spores and cultivars and their distribution in mycelium fragments passively float in different parts of the world make it easy the air and they are often dispersed by air to establish infections by fungal spores currents (Southworth 1974). The distance blown to new territories. Major of transport greatly depends on the spore pathogens of crop plants such as rice, size and shape, the height, thickness and wheat, soybean, oilseed rape, potato as location of the air layer, its physical well as coffee or banana are similar in properties such as temperature, as well as different parts of the globe, in spite of air movements. Most of fungal spores are geographical or political barriers, transported in between local habitats; resulting in no or seedling however, there are strong scientific exchange. These obstacles can be easily evidences on spores being transported overcome by spore invasions with the air within and between geographic regions currents.

Methods used in aerobiology Fungal spores present in the air are Parc Montsouris in Paris in 1883. It was subjected to many studies with the use of an air pump sucking 20 liters of the air spore traps, that may be passive, when via an orifice, with the glass slide spores drop down on certain surfaces or covered with glycerin. This equipment gather in containers, due to their gravity allowed the first calculations of fungal (Koch sedimentation method) or active, spores in the air with high precision; when the collection of spores is hence this researcher is often regarded as connected with swirling or sucking, that the first professional aerobiologist, and allows capturing of higher spore loads one of the main fathers of aerobiology (Fleischer et al. 2006). The most popular and aeromycology (Comtois 1997). Since and advanced methods of spore trapping then, the development of volumetric use volumetric samplers. They allow to methods has been greatly pushed re-calculate the number of observed forward, especially by English spores to a given air unit, mostly 1 cubic researchers Philip Gregory and John meter of the air. The first volumetric Hirst (Hirst 1991). Currently used sampler was used by Pierre Miguel in volumetric spore samplers, such as

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Burkard or Lanzoni apparatus, are based fungal spores into colonies on on models designed by Gregory and microbiological substrates. Moreover, the Hirst. The suction power is standardized, Andersen impactor allows sieving the what allows the comparison of results spores into groups of different sizes. The obtained by different research teams recognition of fungi present in the air are worldwide. then based on traditional visual There are also other types of assessments (Kasprzyk & Worek 2006, apparatus, e.g. the MicroBio or Air Ideal Grinn-Gofroń & Strzelczak 2011, samplers as well as the Andersen Stępalska et al. 2012, Pusz et al. 2013), impactor – the facilities that combine as well as on molecular tools (Kaczmarek volumetric methods with the culture on et al. 2009, Karolewski et al. 2012, media. Both of them allow growing Piliponyte-Dzikiene et al. 2014).

Identification of fungal spores in air with molecular tools The recognition of fungal spores time PCR is designed to quantify the based on spore shape and size is possible numbers of spores or gene copies for such frequent ‘air-flyers’ as Botrytis, (Kaczmarek et al. 2009, Karolewski et Chaetomium, Coprinus, Didymella, al. 2012). Molecular tools allow proper Entomophthora, Epicoccum, Erysiphe, identification of fungal species with Ganoderma, Nigrospora, Pithomyces, similar or identical spores and study the Polythrincium, Stemphylium, Torula, genetic changes in fungal populations, Ustilago and some others (Kasprzyk such as fungicide resistance (Fraaije et 2008). However, numerous spores of al. 2005) or AVR gene alleles different species or even different fungal (Kaczmarek et al. 2014b). Molecular genera can be mixed up in studies based methods allow simultaneous studies of on analysis only. Possibilities several fungal species, allergens or created by impactors allowing to genetic changes. The greatest hope is subculture these fungi partly solve this currently connected with isothermal problem, as they allow identifying fungal methods, such as LAMP, allowing a genera, species and variants below the simplified DNA isolation and greatly species level, but they demand much reducing the possibilities of reaction time and laboratory space. Moreover, inhibition (Jędryczka et al. 2013). great parts of fungal spores present in the Molecular methods are sometimes air are produced by the biotrophs, which criticized for no distinguishing the are unculturable on conventional difference between viable or dead spores, microbiological media. The broadcasting as they both contain DNA. This may be of spores by wind is crucial for all these solved by RNA-based studies, as this species as their survival relies on quick nucleic acid is produced by living cells finding the relevant host. Their detection only and it is rapidly broken down in and proper identification is possible due dead tissues, unlike DNA. Due to to molecular methods. difficulties with RNA stability and PCR-based methods allow precise extraction, current RNA-based studies spore identification s of many fungal are confined to RNA and human species, including the most dangerous pathogens, rather than to plant pathogens plant pathogens (West et al. 2008a). (Schmale et al. 2005). Moreover, recent introduction of Real-

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Most frequent fungal spores in air Although a lot of scientific literature fungi belong to ‘wet spores’, that directly in aeromycology is devoted to fungal relates to their biology. High humidity is plant pathogens, the majority of spores a prerequisite for the successful infection belong to species that do not infect plants of a host-plant. This is why natural directly, but grow saprophytically on mechanisms evolved fruiting bodies with their surfaces. Skjøth et al. (2012) proved layers reacting to the presence of that at the time of crop harvest local load atmospheric water that directly causes of airborne spores greatly increases and it osmotic changes and allows is an agricultural area, which release to air currents. substantially contributes to the sudden Fungal spores of different taxa are raise of fungal spores captured by subjected to specific diurnal and seasonal samplers located in cities. Major part of cycles, which greatly depend on climate, air spora is composed of Alternaria spp. weather conditions, circadian clock and Cladosporium spp., and in general – (changes of day and night) as well as the these two genera constitute the greatest availability of fresh substrates, necessary part of each spore lot in the air, at almost for fungus development (Calderon et al. all geographical latitudes (Kasprzyk 1995). In moderate climate most of 2008) and heights (Pusz et al. 2013). spores occur in summer or early autumn Other frequently encountered spores (Kasprzyk & Worek 2006), whereas in belong to Aspergillus spp., Penicillium tropical areas they are more abundant in spp. and Fusarium spp. Due to great cold seasons of the year (Hasnain 1993). similarities in their spore size and shape Microclimate greatly influences the it is not possible to identify them based release and appearance of spores, what on morphological characteristics. To relates not only to local rainfalls or the properly identify these spores DNA- or effect of ponds, lakes and water RNA-based detection methods are reservoirs, but it may also relate to required, alternatively, the use of suction temperature. The delayed presence of trap which impacts the spores on airborne spores in the season caused by microbiological media. lower temperatures and snow cover were Air contains spores of different found in the mountainous regions (Pusz modes of appearance. Telio- and et al. 2013). On contrast, in ‘urban heat urediniospores of rusts (e.g. Puccinia, islands’ plants usually produce more Ustilago or Melampsora spp.), as well as pollen and their seasonal occurrence Alternaria, Cladosporium, Epicoccum or starts earlier and lasts longer (Calderon et Drechslera are present in the air of low al. 1997), what partially applies also to humidity, and therefore they are called the abundance of fungal spores. ‘dry spores’, whereas Didymella, Microclimate and local turbulences make Fusarium, Ganoderma, Gliocladium, it difficult to accurately predict the Leptosphaeria or Verticillium fungi occurrence of spores. The studies are release spores after rainfall events, that easier when airborne fungal spores are puts them to the group of fungi transported by big air currents, which can producing ‘wet spores’. In general, be tracked by back-trajectories (Sadyś et numerous of plant infecting al. 2014).

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Disease forecasting systems Forecasting of spore release, based on Poland runs the System for biology of a particular fungal taxon and Forecasting Disease Epidemics SPEC the weather finds direct use in plant and (Jędryczka et al. 2012) – the third human protection against infectious world’s biggest system based on diseases. The systems check if a regional aerobiological methods. The system has or local weather favored the production been constantly operating since 2004 and release of pathogen inoculum and the (Jędryczka et al. 2006). Similar attempts infection of the host (West et al. 2008b). have been recently undertaken in the Disease forecasting systems used in Czech Republic (Jędryczka et al. 2010). modern agriculture are usually based The studies concentrate on Leptosphaeria either on mathematical models, which maculans and L. biglobosa – the were built up following the experiments pathogens infective to oilseed rape on pathogen biology, or they refer to (Brassica napus), which belongs to one stages of development of plant of top cash crops. Air samples captured pathogens, controlled at time points that with volumetric spore traps are are crucial for plant epidemics. The quantified with light microscope and effective plant control is currently a molecular techniques (Kaczmarek et al. compulsory policy of the European 2009, 2014b). Airborne spores that form Union (Kaczmarek et al. 2014a). The inoculum responsible for disease challenge of plant disease control is a key epidemics allow predicting the risk of component of increasing food production yield losses as well as its quality. Timely and food security (West 2014). It was applications of fungicides are beneficial proven that the use of decision support to agriculture. High precision of plant systems brings economic rewards to protection treatments, based on farmers and better protects the aerobiological data, allows combating the environment. pathogen with the highest efficiency.

Outdoor and indoor air spora allergenic to humans High concentration of airborne spores proteins that can be detected with ELISA may lead not only to plant diseases, but tests or other molecular diagnostic often cause skin, eye or nasal irritation methods. Initially the detection and diseases of human respiratory concerned Penicillium roqueforti, the systems, resulting in shortness of breath, fungus responsible for food spoilage and alveolitis and . Rapiejko et al. serious diseases of cheese workers (2004) elaborated threshold values for (Campbell et al. 1983). The symptoms the spores of Alternaria and ranged from cough, dyspnea and malaise Cladosporium spp. necessary to evoke to reduced lung volumes and hypoxemia. allergic symptoms. In case of the other The studies revealed that serum and fungi such values have not been lavage fluids of the patient contained published. It is also clear that these antibodies to P. roqueforti. This is one of numerical values are only indicative numerous cases allowing understanding a figures, and the allergic reaction greatly serious influence of airborne fungi on depends on patients’ age, health human health, which started a series of condition and numerous individual studies on indoor air spora in numerous characteristics. Modern traps enable the countries, including Poland (Lipiec 1997, collection of with allergenic Górny & Dutkiewicz 2002, Lipiec &

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Samoliński 2002, Karwowska 2003, “Riese” located in underground complex Filipiak et al. 2004, Stryjakowska- Osówka in the Sowie Mountains showed Sekulska et al. 2007, Dumała & that Cladosporium spp. were most Dudzińska 2013). Since then, the whole frequently isolated both from internal and selection of different apparatus and external atmosphere (Pusz et al. 2014b). methods has been elaborated to monitor However, in shafts of copper mine fungal spores and allergens in the air, located in Lubiń mining site (property of ranging from static samplers to minute, KGHM Polska Miedź SA) the most portable instruments. Most studies were numerous fungi belonged to Penicillium done in public buildings such as spp. and Aspergillus spp., with P. universities, schools and hospitals. The notatum and P. urticae found as best monitoring revealed that the adapted to grow in these specific concentration of only conditions (Pusz et al. 2014a). rarely exceeded its recommended limits. Significant differences between the However, some of fungal species present composition and size of fungal species in the indoor air of studied rooms could between the shafts and sample collection negatively affect human health. sites supported the hypothesis on The compositions of fungal air spora substantial influence of microclimate on in man-made places greatly differed, fungal air spora. Fortunately, in this even at sites located in seemingly similar particular case the concentration of conditions. Speleomycological research fungal spores also did not present a done in unfinished Nazi military complex health risk to the mine workers.

Concluding remarks The potential of fungal spores in the (2012), it is clear that aeromycology is air is in contrast to their ‘invisibility’ connected to numerous basic and applied caused by vast dispersion and small size sciences, such as allergology, of particular spores. However the impact bioclimatology, biological pollution, on humans and their economy may be biological warfare and terrorism, enormous, with great influence on such mycology, biodiversity studies, ecology, crucial branches as agriculture or human plant pathology, microbiology, indoor air safety. Based on a review on primary quality, industrial aerobiology, biological particles in the speleology, cultural heritage and many atmosphere, written by Després et al. other disciplines.

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Streszczenie Powietrze jest naturalnym środowiskiem dla zarodników licznych rodzajów i gatunków grzybów. Pomimo niewielkich rozmiarów i znacznego rozproszenia mają one wielki wpływ na zdrowie ludzi i różne kierunki ich działalności, w tym w szczególności na produkcję rolniczą. Badania nad zarodnikami grzybów stanowiącymi część aeroplanktonu są przedmiotem aeromykologii. Niezależnie od szerokości geograficznej i wysokości nad poziomem morza w powietrzu szczególnie często występują grzyby z rodzajów Cladosporium i Alternaria, a ich źródłem jest najczęściej środowisko rolnicze. Innymi często notowanymi rodzajami grzybów, których zarodniki występują w powietrzu są m.in. Aspergillus, Penicillium, Fusarium, Sclerotinia i Ganoderma. Stężenie zarodników w powietrzu jest ściśle uzależnione od obfitości ich tworzenia w danym okresie, co jest pochodną regionu geobotanicznego, szaty roślinnej, stopnia zurbanizowania danej lokalizacji, warunków klimatycznych, pory roku, aktualnej pogody, siły i kierunku wiatru, lokalnego mikroklimatu i wielu innych czynników. Zmiany wilgotności powietrza wpływają na stężenie zarodników różnych rodzajów grzybów, określanych na tej podstawie jako „suche” (Alternaria, Cladosporium, Puccinia, Ustilago, Melampsora, Epicoccum, Drechslera) lub „mokre” (Didymella, Fusarium, Ganoderma, Gliocladium, Leptosphaeria, Verticillium). Badania składu rodzajowego i gatunkowego prowadzone są przy zastosowaniu różnego rodzaju chwytaczy zarodników, a identyfikacja wizualna na podstawie morfologii kolonii grzyba oraz kształtu i wymiarów zarodników uzupełniana jest obecnie przez wyjątkowo czułe metody detekcji molekularnej, specyficzne względem rodzajów, gatunków, chemotypów, a nawet składu genów i kompozycji poszczególnych alleli. Monitoring aerobiologiczny znajduje bezpośrednie wykorzystanie w epidemiologii chorób ludzi (alergologia) i roślin uprawnych (systemy wspierania decyzji w ochronie roślin uprawnych). Badania z zakresu aeromykologii znajdują zastosowanie w tak

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