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Characteristics and taxonomy of Cladosporium

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 PRACE POGLDOWE / REVIEW ARTICLES Mikologia Lekarska 2012, 19 (2): 80-85
Copyright 2012 Cornetis
www.cornetis.pl
ISSN 1232-986X

Characteristics and taxonomy of Cladosporium fungi

Charakterystyka i taksonomia grzybw z rodzaju Cladosporium

Rafa Ogrek1, Agnieszka Lejman2,Wojciech Pusz1, Anna Miuch1, Paulina Miodyska1

1
Division of Plant Pathology and Mycology, Department of Plant Protection, Wrocaw University of Environmental and Life Sciences, Poland
2
Department of Agroecosystems and Green Areas Management, Wrocaw University of Environmental and Life Sciences, Poland

ABSTRACT
Fungi 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

STRESZCZENIE
Grzyby z rodzaju Cladosporium wystpuj powszechnie wwielu rejonach wiata, s to organizmy kosmo-
polityczne. Ich zarodniki mona spotka wpowietrzu, glebie i wodzie. Powszechnie izolowane s rw-
nie z pomieszcze mieszkalnych i uytku publicznego oraz z produktw ywnociowych. Niektre ga-
tunki s patogenami rnych rolin, powodujc wane gospodarczo choroby rolin, ainne maj tylko
znaczenie endemiczne. Pospolicie wystpuj take jako saprotrofy. U zb mog powodowa czer
zb, u rolin dyniowatych parcha dyniowatych, u pomidora brunatn plamisto lici pomidora. U ludzi
powoduj gwnie reakcje alergiczne, ktre prowadz niekiedy do astmy. Mog te bardzo rzadko powo-
dowa zakaenia oportunistyczne i dotycz one gwnie osb z obnion odpornoci. Istniej jednak
doniesienia o zakaeniach zdrowych osb m.in. przez Cladosporium carrionii, ktry moe wywoywa
zmiany typu chromoblastomikozy.

SOWA KLUCZOWE: Cladosporium, gatunki, alergeny

Introduction Nowadays, allergies in humans caused by fungi are a very

Fungi as akingdom 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.
80
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,

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 aparallel 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
Ogrek R., Lejman A., Pusz W. i wsp.
Charakterystyka i taksonomia grzybw z rodzaju Cladosporium
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 asho-
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 aday has avery 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 afew 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 achronic 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, 81
 Ogrek R., Lejman A., Pusz W., et al.
Characteristics and taxonomy of Cladosporium fungi Mikologia Lekarska 2012, 19 (2)

Fig. 1. Black point on wheat Fig. 2. Scab disease on cucumber leaves caused by Cladosporium cucumerinum
Ryc. 1. Czer zb na pszenicy Ryc. 2. Parch dyniowatych na liciach ogrka spowodowany przez Cladosporium cucumerinum

Fig. 3. Chemical structure of mycotoxin emodin [32] Fig. 4. Chemical structure of mycotoxin cladosporin [33]
Ryc. 3. Struktura chemiczna mitoksyny emodlin [32] Ryc. 4. Struktura chemiczna mitoksyny cladosporin [33]

Fig. 5. Culture of Cladosporium herbarum in Petri dish on PDA medium

Ryc. 5. Hodowla Cladosporium herbarum na szalce Petriego na podou PDA

subcutaneous and systemic changes in the cornea of the eye. The

superficial changes are known as tinea nigra and may be caused
Fig. 6. Conidial spores of Cladosporium herbarum
by Cladosporium castellani Borelli & Marcano and Cladosporium Ryc. 6. Zarodniki konidialne Cladosporium herbarum
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 aresult 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 Fig. 7. Sporulation in Cladosporium herbarum
82 skin. High concentrations of mycotoxins can cause strong dama- Ryc. 7. Zarodnikowanie Cladosporium herbarum

Table I: Some antigens of Cladosporium herbarum [3]
Tabela I: Niektre antygeny Cladosporium herbarum [3]
Alergens symbol Molecular mass [kDa] Properties
Symbol alergenu Masa czsteczkowa [kDa] Waciwoci more than five hundred taxa have been attributed to Cladospo-
Cla h 1 13
Cla h 2 23
Cla h 3 53 Aldehyde dehydrogenase
Dehydrogenaza aldehydowa
Cla h 4 11 Acidic ribosomal protein P2
Kwane biako rybosomalne P2
Cla h 5 22 Protein YCP4
Biako YCP4
Cla h 6 48 Enolase
Enolaza
Cla h 12 11 Acidic ribosomal protein P1
Kwane biako rybosomalne P1
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 adiar-
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 amutagenic 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 asmall (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 aslightly 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
Ogrek R., Lejman A., Pusz W. i wsp.
Charakterystyka i taksonomia grzybw z rodzaju Cladosporium
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,
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 aturf, 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
across-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 m
long and 3-6 m wide, with terminal and intercalary swellings
(7-9 m 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 afinely granulate or spiny
wall, of very different diameters and lengths [44]. One-celled,
reaching 5,5-133,8-6 m (fig. 7). The similar C. murorum has been
distinguished from C. herbarum on account of its shorter terminal
conidia 3-7 m 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 m
long but usually much shorter, 2-6 m 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) m.
The most similar species to C. cladosporioides is C. cucumerinum,
which has woolly, pale grey-green colonies [10].
83
 Ogrek R., Lejman A., Pusz W., et al.
Characteristics and taxonomy of Cladosporium fungi
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 12-474-10 m in diameter
and 1- to 4-celled, usually colorless or yellow-brown and have
athick cell wall [16].
Cladosporium cucumerinum spots are 3-4 mm in diameter and
might ooze agummy 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 m in
width. The ramoconidium was mostly single-celled showing 9,0-
27,5 2,5-5,0 m (mean value, 15,24,3 m) 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 5-252-6 m (mean value, 10,64,1 m). 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
athreat 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 abasement 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 aday for 30 minutes) and to install agood 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
awalk 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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