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Characteristics and taxonomy of Cladosporium fungi

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Mikologia Lekarska 2012, 19 (2): 80-85Copyright © 2012 Cornetis

www.cornetis.plISSN 1232-986X

PRACE POGLĄDOWE / REVIEW ARTICLES

Characteristics and taxonomy of Cladosporium fungiCharakterystyka i taksonomia grzybów z rodzaju Cladosporium

Rafał Ogórek1, Agnieszka Lejman2,Wojciech Pusz1, Anna Miłuch1, Paulina Miodyńska1

1 Division of Plant Pathology and Mycology, Department of Plant Protection, Wrocław University of Environmental and Life Sciences, Poland2 Department of Agroecosystems and Green Areas Management, Wrocław University of Environmental and Life Sciences, Poland

ABSTRACTFungi of the genus Cladosporium are common in many areas of the world, they are cosmopolitan organi-sms. Their spores can be found in air, soil and water. Also, they are commonly isolated from accommoda-tion and public use areas and from food products. Some species are pathogens of various plants, causing economically important plant diseases and others have only endemic importance. Commonly they occur as saprotrophs. In the cereals fungi can cause black point of cereals, in Cucurbita they can cause scab of cucurbits and in tomato brown spots on the leaves. In humans, they mainly cause allergic reactions which sometimes lead to asthma. They can cause rarely opportunistic infections, this is related mainly to people with compromised immune systems. There are also reports about infections in healthy people by Clado-sporium carrionii, which may cause lesions, for example chromoblastomycosis.

KEY WORDS: Cladosporium, species, allergens

STRESZCZENIEGrzyby z rodzaju Cladosporium występują powszechnie w wielu rejonach świata, są to organizmy kosmo-polityczne. Ich zarodniki można spotkać w powietrzu, glebie i wodzie. Powszechnie izolowane są rów-nież z pomieszczeń mieszkalnych i użytku publicznego oraz z produktów żywnościowych. Niektóre ga-tunki są patogenami różnych roślin, powodując ważne gospodarczo choroby roślin, a  inne mają tylko znaczenie endemiczne. Pospolicie występują także jako saprotrofy. U zbóż mogą powodować czerń zbóż, u roślin dyniowatych parcha dyniowatych, u pomidora brunatną plamistość liści pomidora. U ludzi powodują głównie reakcje alergiczne, które prowadzą niekiedy do astmy. Mogą też bardzo rzadko powo-dować zakażenia oportunistyczne i dotyczą one głównie osób z obniżoną odpornością. Istnieją jednak doniesienia o zakażeniach zdrowych osób m.in. przez Cladosporium carrionii, który może wywoływać zmiany typu chromoblastomikozy.

SŁOWA KLUCZOWE: Cladosporium, gatunki, alergeny

Introduction

Fungi as a kingdom were isolated in 1969 by R.H. Whittaker and include over 81000 highly diverse species. Most of them develo-ped in terrestrial habitats. Fungi grow best in moist habitats, because they require water to live. Optimum pH for fungal growth is 5.6, but many of them can tolerate values in the range 2-9. Low sensitivity to changes in osmotic pressure causes the ability of fungi to grow in solutions with high salt or sugar and they can attack frozen food [1]. Fungi, due to their requirements of life, occupy the microenvironment in which people live and they have an influence on quality of life [2]. Fungi can cause internal and external infections and also can be allergenic factors in humans and animals.

Nowadays, allergies in humans caused by fungi are a  very serious problem. However, the first reports on the impact of fila-mentous fungi on human health come from books of the Old Testament. Whereas the relationship between exposure to fungi and bronchial asthma for saw the first time John Floyer in 1726 [3].

Fungal spores present in the air cause allergies. They can mani-fest in the form of food allergy, contact allergy, allergies to anti-biotics or an allergic reaction in the case of fungal infection exi-sting in the body of focus. It should be noted that fungal spores are among the most widely represented biological molecules in atmospheric air. They considerably outweigh the number of pol-len grains present in the air [2]. Symptoms of the respiratory sys-tem of an organism caused by the response to the fungi allergens are much stronger than to other allergens commonly encounte-red in the environment. The reason for this is probably that fungi,

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except allergenic proteins, have the ability to reproduce and infect the skin and are able to colonize the respiratory system [4]. Moreover, they can synthesize secondary metabolites such as toxins, hypo-allergenic enzymes and volatile organic compounds and functional non-protein components of the cell wall (glucans and chitin) [5-7]. Another aspect are the cross autoimmune reac-tions caused by high homology to fungal antigens of some human proteins which occur especially in patients with chronic asthma. Taking into account all of these mechanisms, it was hypothesized that the damaging effects of fungi in the respiratory system are associated with a parallel induction of allergic inflammation and damage to respiratory epithelium cells by the action of proteins and not allergenic toxins [8].

From allergological point of view it is important that species of fungi belong to different taxonomic groups [9].The majority inc-ludes: Alternaria spp., Cladosporium spp., Penicillium spp., Asper-gillus spp. and also fungi of the genus Mucor, Botrytis, Fusarium, Pullularia, Curvularia, Phoma and Rhizopus. Typically, allergies are associated with hypersensitivity to several species of fungi. Coexi-stence of hypersensitivity to various species is probably in most cases associated with parallel allergy and not with the cross-reactivity [2].

Biology, ecology and pathogenicity of Cladosporium spp.

Fungi of the genus Cladosporium Link ex Fr. are common in many parts of the world, they are cosmopolitan organisms. Their spores can be found in air, soil and water [10]. Commonly they are also isolated from residential and public use areas and from food products [11, 12]. Cladosporium spp. requires cool, damp weather conditions for vivid growth, sporulation, spore release, germina-tion and disease development. These fungi are active at low tem-peratures and high humidity [13].

Some species are pathogens to various crops, they can cause economically important plant diseases and others have only endemic importance. Fungi commonly occur as saprotrophs on plant vestiges [14]. These fungi can cause diseases of plants, often with different names, depending on the infected plants and the type of symptoms. In the cereals fungi can cause black point of cereals, in Cucurbita they can cause scab of cucurbits and in toma-to brown spots on the leaves [15, 16].

Cladosporium fulvum Cooke can cause brown spots on tomato leaves. This disease occurs on tomato crops in greenhouses and poly-tunnels. In case of favorable conditions, it can cause reduc-tion of yield by destroying the leaves and (killing) plants. The spe-cies of this fungus was described in 1883 in South America. In Poland it has been known since 1930. Currently, the disease has low interest, which is caused by cultivation of resistant cultivars and improving conditions in greenhouses and poly-tunnels. Reproduction of this pathogen is unknown, only the results of molecular studies enabled classification of teleomorph genus Davidiella [16].

Cladosporium herbarum (Persoon) Link with other fungi (Alter-naria spp. and Epicoccum spp.) can cause black point of cereals (fig. 1). This disease is very unusual, because it usually occurs on premature dried plants or mature plants. It causes mainly reduc-tion of grain quality, where are accumulated mycotoxins secreted by fungi growing on the surface or in the tissues. In this pathogen reproduction could not be determined either, only the results of

molecular studies enabled classification of teleomorph genus Davidiella [16].

Cladosporium cucumerinum Ell. et Arth. has been known as an important pathogen which can cause scab disease in cucumber all over the world [17, 18]. The symptoms of the disease can affect leaves, petioles, stems and fruits (fig. 2). Water-soaked spots occur on leaves and runners. These spots eventually turn from grey to white. The centre of the spots could then drop out to give a “sho-t-holed” appearance. Lesions on the fruit are often connected with anthracnose. These spots are 3-4 mm in diameter and might ooze a  gummy substance. The spots can then be invaded by secondary rotting bacteria which cause the spots to smell [19].

Cladosporium spp. can cause allergic reactions in humans, which sometimes leads to asthma. Rarely, they can cause oppor-tunistic infections, this is related mainly to people with compro-mised immune systems such as patients with hematological dise-ases or AIDS. There are also reports about infections in healthy people by Cladosporium carrionii Trejos, which may cause lesions, for example chromoblastomycosis [20].

Studies of atmospheric air of various regions of Europe show that the spores of Cladosporium spp. dominate in 80% of all the caught spores and the spores of Alternaria spp. in about 10% [21]. However, the level of concentrations of Cladosporium spores in the air (in 1m3) in a day has a very large variation over the year: from zero to several thousand spores. In European countries, the peak of season of Cladosporium and Alternaria sporulation is in the months from June to September, when the concentration of Cladosporium spores reaches several thousand per cubic meter of air, and Alternaria spores – a few hundred [21, 22]. Despite the gre-ater occurrence of the spores of Cladosporium spp., the spores of Alternaria spp. are more allergenic. The number of spores neces-sary to induce symptoms of allergic respiratory system disease in most patients with hypersensitivity to these allergens for the Polish population was estimated at 2800 spores in 1 m3 of air for Cladosporium spp. and only 100 for the spores of Alternaria spp. [23]. The reason for this is probably that about 80% of A. alterna-ta conidia occuring in the air are alive cells, while C. herbarum only 20-30% of living cells [24]. Another differentiating allergenicity factor of individual species of fungi is how easily spore allergens may be released in contact with the surface of the mucosa. It is considered that the spores of A. alternata allergens are released with ease, while the allergens from spores of other species such as Aspergillus fumigatus require their physical damage. Cell walls of spores determine the availability of allergen for the mucosal spore after getting to the respiratory system [2].

Opportunistic infections of people caused by fungi of Clado-sporium spp. are mainly chromoblastomycosis and phaeohypho-mycosis. Chromoblastomycosis is a chronic infection of the skin and subcutaneous tissue. For the first time, this mycosis was described by Rudolph in 1914. This disease can occur at any lon-gitude and most of reported cases are related to farmers. Patho-logical changes are usually located in the lower limbs, sometimes the upper limbs, less frequently in other areas of the body. The first disease symptoms are small, scaly papules and nodules. In the course of the disease chronic ulcers can arise, covered with dry scabs. The disease is chronic and can lead to lymphatic stagna-tion. Whereas Cladosporium cladosporioides (Fresen.) GA de Vries and Cladosporium bantianum (Sacc.) Borelli can cause phaeohy-phomycosis. For the first time the name of the disease was intro-duced in 1974 by Ajello. The Disease appears as dermal infections,

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subcutaneous and systemic changes in the cornea of the eye. The superficial changes are known as tinea nigra and may be caused by Cladosporium castellani Borelli & Marcano and Cladosporium wernecki Horta. That kind of mycosis is present mainly in warm countries [20]. Other species, such as C. cladosporioides and C. bantianum, can cause subcutaneous and systemic forms of pha-eohyphomycosis [25]. Subcutaneous form is the result of post trau-matic implantation of the fungus [26]. In system infections, lesions concern the brain and are caused mainly by C. bantianum [27].

Fungi of the genus Cladosporium, like other microscopic fungi, secrete various secondary metabolites such as mycotoxins. Most of mycotoxins are not susceptible to heat, and as a result they are stable during normal preparation processes of food and feeding. They can cause many animal diseases and health problems in humans. They penetrate into the body not only through the gastrointestinal systems, but also by inhalation and through the skin. High concentrations of mycotoxins can cause strong dama-

Fig. 1. Black point on wheatRyc. 1. Czerń zbóż na pszenicy

Fig. 5. Culture of Cladosporium herbarum in Petri dish on PDA mediumRyc. 5. Hodowla Cladosporium herbarum na szalce Petriego na podłożu PDA

Fig. 3. Chemical structure of mycotoxin emodin [32]Ryc. 3. Struktura chemiczna mitoksyny emodlin [32]

Fig. 2. Scab disease on cucumber leaves caused by Cladosporium cucumerinumRyc. 2. Parch dyniowatych na liściach ogórka spowodowany przez Cladosporium cucumerinum

Fig. 6. Conidial spores of Cladosporium herbarumRyc. 6. Zarodniki konidialne Cladosporium herbarum

Fig. 7. Sporulation in Cladosporium herbarum Ryc. 7. Zarodnikowanie Cladosporium herbarum

Fig. 4. Chemical structure of mycotoxin cladosporin [33]Ryc. 4. Struktura chemiczna mitoksyny cladosporin [33]

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Ogórek R., Lejman A., Pusz W. i wsp.Charakterystyka i taksonomia grzybów z rodzaju Cladosporium

ge to internal organs, which can lead to severe clinical diseases, whereas low concentrations of mycotoxins may cause their accu-mulation, which with time can lead to chronic diseases in humans and animals such as kidney and liver cancers [28]. Therefore, it is important to establish the type of toxin and its concentration in plant products [29]. The main mycotoxins which are secreted by fungi of Cladosporium spp. are emodin (fig. 3) and cladosporin (fig. 4). Emodin (2-methyl-4,5,7-trihydroxyanthraquinone) is a diar-rheagenic toxin produced by C. fulvum and C. cladosporioides [30, 31]. Cladosporin (3,4-dihydro-6,8-dihydroxy-3-(6-methyltetra-hydro-pyran-2-ylmethyl)isocoumarin) is a mutagenic and cytoto-xic secondary metabolites product produced by C. cladosporioides [32, 33].

Studies conducted in Poland have shown that most allergies due to the mold allergens are caused by fungi of the genera Alter-naria and Cladosporium [8, 34]. Fungi allergens biochemically belong to different categories (proteases, glycosidases, protein components, proteins of oxidative stress and enzymes involved in the process of gluconeogenesis and pentose cycle) [3]. At least 60 antigens derived from C. herbarum were detected by CIE, and 36 were allergenic by CRIEN – some of them are shown in table I [35]. Allergen Cla h 1 (Cla h I or Ag-32) is a small (13-kDa) acidic aller-gen composed of five isoallergens (pI 3.4 to 4.4). Cla h 2 (Cla h II or Ag-54) is a slightly larger (20- to 23-kDa), less acidic (pH 5.0) gly-coprotein containing 80% carbohydrate (mannose-galactose-glu-cose, 1:0.6:1.3) [36-38]. After carbohydrate and protein moieties were separated, only the protein retained IgE-binding properties; interestingly, this binding was stronger than that for native Cla h 2. Four cDNA clones from Cladosporium herbarum that code for allergens were isolated recently. Sequence homology indicated that these allergens are aldehyde dehydrogenase (Cla h 3; 53 kDa), P2 ribosomal protein (Cla h 4; 11 kDa) and P1 ribosomal protein (Cla h 12; 11 kDa), YCP4 yeast protein (Cla h 5; 22 kDa), and enola-se (Cla h 6; 48kDa). These well-characterized allergens should prove extremely useful as models for allergen analysis of this ubi-quitous fungus spore type [39].

Taxonomy and identification of Cladosporium spp.

The genus Cladosporium was described by H.F. Link in 1816 with C. herbarum as type species. Surveys of the generic history of Cladosporium were conducted by De Vries in 1952 and David in

1997. Early descriptions of Cladosporium were rather vague and the delimitations from similar genera obscure, e.g. Nees (1817), Corda (1837), Fries (1832) or Lindau (1907). Since its introduction, more than five hundred taxa have been attributed to Cladospo-rium. Due to the imprecise circumscription of Cladosporium, it is not surprising that numerous superficially similar but unrelated hyphomycetes have been assigned to this genus, making it very heterogeneous [40].

These fungi are commonly found in the conidial stage (ana-morph), while the perfect stage of fungi (teleomorph) is forming rarely. However, the results of molecular studies enabled classifi-cation of their teleomorph to Davidiella [16]. Previously, this genus was classified into phylum Deuteromycota (Fungi imperfec-ti), class Hyphomycetes, order Moniliales and family Dematiaceae (dark-colored fungi) [41, 42]. Now, due to large changes in taxo-nomy of fungi, this genus is recognized as phylum Ascomycota, class Dothideomycetes, order Capnodiales and family Davidiellace-ae [43].

Cladosporium spp. grow moderately fast on PDA medium at 25 °C and form velvety, mealy, gray-green to olivaceous-green and reverse black colonies. Most species do not grow at temperature above 35 oC. Fungi of this genus hydrate gelatin, they are not ther-motolerant and they are sensitive to benomyl [43]. The hyphae of these fungi are creeping, septate on the surface or in the substra-te. Conidiophores almost erected, branched, and floccose, it often forms a turf, it is olive-colored [44]. Blastospores are 1- or 2-celled, sometimes 3-celled, variable in shape and size [15]. Generally, conidia globose and ovate when one-celled, then usually with a cross-wall, commonly greenish [44].

In determining species of the genus Cladosporium, it is impor-tant to understand the etiology of these fungi and, what is more, that the harmfulness of each species is different. Therefore, the genus Cladoporium, which most often occurs on crops, was cha-racterized.

Cladosporium herbarum colonies reach 3-7 cm in diameter in ten days on MEA at 20oC, olivaceous-green to olivaceous-brown, velvety, reverse olivaceous-black (fig. 5). Conidiophores to 250 μm long and 3-6 μm wide, with terminal and intercalary swellings (7-9 μm diameter), geniculate and elongated (fig. 6) [10]. Conidia terminal, by extension of the tip falsely lateral, on short knee-like swellings, single or at times in chains, of various shapes, elonga-ted, oval, and then usually one-celled, or cylindrical-ellipsoidal and then with one- to four-septa, smoky-brown or olive-green, slightly constricted at the septa, with a finely granulate or spiny wall, of very different diameters and lengths [44]. One-celled, reaching 5,5-13×3,8-6 μm (fig. 7). The similar C. murorum has been distinguished from C. herbarum on account of its shorter terminal conidia 3-7 μm long and also usually, the absence of septate coni-dia [10].

Cladosporium cladosporioides colonies reach 3 – 4 cm in diame-ter in ten days on MEA at 20 oC, olivaceous-green to olivaceous-brown, velvety, reverse olivaceous-black. Conidiophores are 350 μm long but usually much shorter, 2-6 μm wide, acropleurogenous branches that bear numerous conidial chains arising below septa, but without swelling and sympodial elongations. Conidia are ellipsoidal to lemon-shaped, mostly smooth-walled, rarely minu-tely verrucose, olivaceous-brown, one-celled 3-7 (-11)×2-4 (-5) μm. The most similar species to C. cladosporioides is C. cucumerinum, which has woolly, pale grey-green colonies [10].

Table I: Some antigens of Cladosporium herbarum [3]Tabela I: Niektóre antygeny Cladosporium herbarum [3]

Alergens symbol Symbol alergenu

Molecular mass [kDa]Masa cząsteczkowa [kDa]

Properties Właściwości

Cla h 1 13 –

Cla h 2 23 –

Cla h 3 53 Aldehyde dehydrogenaseDehydrogenaza aldehydowa

Cla h 4 11 Acidic ribosomal protein P2Kwaśne białko rybosomalne P2

Cla h 5 22 Protein YCP4Białko YCP4

Cla h 6 48 EnolaseEnolaza

Cla h 12 11 Acidic ribosomal protein P1Kwaśne białko rybosomalne P1

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Allergy is caused mostly by C. herbarum and C. cladopsorioides. These fungi are greatly different in the fact that hyphal cells and conidia of C. cladosporioides are generally 1- or rarely, 2-celled and C. herbarum 2- or 4- celled [43].

Conidiophores of C. fulvum are concentrated in the dark colo-red tufts and divided into cells. Blastospores are formed on the top and side branches. The spores are 12-47×4-10 μm in diameter and 1- to 4-celled, usually colorless or yellow-brown and have a thick cell wall [16].

Cladosporium cucumerinum spots are 3-4 mm in diameter and might ooze a gummy substance. The spots can then be invaded by secondary rotting bacteria which cause the spots to secrete smell [19]. The fungal conidiophore was characterized by pale oli-vaceous brown color, and variable length of about 3~5 μm in width. The ramoconidium was mostly single-celled showing 9,0-27,5 × 2,5-5,0 μm (mean value, 15,2×4,3 μm) in length, with 0-2 septa. Conidia were formed in long branched chains, and coni-dium was ellipsoidal, fusiform or subspherical single cell mostly without septum (occasionally with 1 septum). The length of the conidium was 5-25×2-6 μm (mean value, 10,6×4,1 μm). Colonies on PDA were densely packed with greenish black color. These morphological characteristics of the isolate were almost identical to C. cucumerinum [45].

Conclusion

Fungi of the genus Cladosporium are cosmopolitan organisms. Their spores can be found in air, soil and water. However, some genera are pathogens of various plants and people.

Particularly C. cladopsorioides and C. herbarum are some of the most common aeroallergens next to Alternaria spp. We can meet them in the external environment and in accommodation spaces, offices and warehouses. Their allergic potential is lower than the fungi of the genus Alternaria. However, being in locations charac-terized by a  high concentration of spores of the fungus poses a threat to human health.

People who experience allergic symptoms should avoid con-tacting with the fungus and reduce its presence in the room. It may be useful to gain some knowledge about the biology of these fungi (spread, overwintering, plant diseases caused by them, atmospheric conditions conducive to their development) [46].

In order to reduce the development of Cladosporium spp. in buildings, the flat, apartment building or a basement should be made dry, because high humidity stimulates/encourages growth of all types of fungi. Therefore, it is recommended to air the rooms (2 times a day for 30 minutes) and to install a good ventilation in the bathroom, because the humidity is always higher there than in other areas. Another thing is to review and clean air conditio-ning systems, because the wrong conservation of air conditioning system causes an increasing fungal air pollution [47]. People susceptible to allergies should avoid working at the allotment and in the garden. During the rainless weather, the best time to go for a walk is in the morning due to the lowest concentration of fun-gal spores in the air. It is also useful to order tests for the presen-ce of fungi in the apartment.

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Received: 2012.03.20. Approved: 2012.06.08.Conflict of interests: none declared

ADDRESS FOR CORRESPONDENCE:Rafał Ogórek, M.Sc. Eng.

pl. Grunwaldzki 24a

50-363 Wrocław, Poland

tel.: +48 511 078 318

e-mail: rafal.ogorek@up.wroc.pl

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