Ulocladium chartarum

Ulocladium chartarum on gypsum boardUlocladium chartarum on wood"Ulocladium chartarum on a ceiling tileUlocladium chartarum on EM agarUlocladium chartarum on RB agarUlocladium chartarum - Microscopy (EM Culture)

Basics

The International Mycological Association recognises, in its fungal database, 26 named species within the genus Ulocladium{3971}. There are 15 named species of Ulocladium registered with the international data bank of the Universal Protein Resource agency (Uniprot) as well as over 20 unnamed strains {3318}.

The species associated with indoor contamination and health effects are mainly U. chartarum, U. atrum and U. botrytis, although most fungi of this genus alluded to in articles relating to environmental exposure are only noted as Ulocladium sp. 

Taxonomy

Kingdom Fungi Order Pleosporales
Phylum Pezizomycotina Family Pleosporaceae
Class Dothideomycetes Genus Ulocladium

Ulocladium chartarum is an anamorph fungus: no teleomorph stage has been reported.

Ulocladium species closely resemble certain species of Alternaria and have sometimes been classified as such in the past {1831}. In fact, Ulocladium spp. are phylogenetically related to Alternaria spp., resulting in some species having been misidentified.

Habitat/Ecology

Ulocladium is a genus of ubiquitous saprophytic and widely distributed moulds, found in soil, wood and decaying plants. Certain species are plant pathogens and food spoilers; when found on food and feedstuffs, it is mostly on nuts, beans and cereals. Outdoors, Ulocladium spp. are often found on dead vegetation, in soil, air and dust.

A meta-analysis conducted in 2007 revealed that airborne Ulocladium species are found in both outdoor and indoor environments in (numerous, various) countries {1830}; Ulocladium spp. were found in the outdoor environment in 42% of the 51 studies compiled. For instance, species of Ulocladium were found in outdoor air in subtropical countries as well as associated with outdoor settled dust in desert countries {1841; 1830}. Conversely, sampling of outdoor air in Athens revealed that Ulocladium was only a minor contaminant, being isolated in 0.56% of samples {1282}.

Growth requirements

Species of Ulocladium grow at temperatures ranging from 5 to 34 °C {725}.  Indoors, Ulocladium sp. is considered a tertiary coloniser and an indicator of indoor moisture problems {3020}; in fact, it requires a high water environment to germinate and grow, although it can survive the stress of short drier periods. 

Ulocladium appears to be able to grow at lower humidity levels if maintained at these levels over time; growth has been observed on wallpaper in an environment exhibiting a relatively constant relative humidity (RH) above 75% {3729}.

Water Activity:    Aw:  0.89-0.90     {3729; 3969; 3863}.

Growth on building materials or indoor environment

Ulocladium sp. has been found indoors on water-damaged building materials. It has also been isolated from paper, textiles fibres. U. chartarum is found in house dust, mattress dust and in domestic air conditioners {1835; 725; 724}.

Under humid conditions, in the indoor environment, Ulocladium has been found on painted surfaces, tapestry and on water-damaged building materials {725}. In a study by  Gravesen et al., Ulocladium (U. chartarum and U. oudemansii ) was found to be the fourth most prevalent fungus (21%) in 72 samples retrieved from 23 mould-infected public buildings in Denmark {605}.

Some studies reported that Ulocladium sp. was present on building materials but not in the air, possibly indicating that spores from certain species may not be easily released into the air {1830}. For instance, it was found in very limited amounts in house dust of Danish schools (frequency less than 2%).

Nevertheless, the fact that Ulocladium can produce strong toxic endo­meta­bolites when grown on synthetic medium may mean that it could contribute to poor indoor air quality and health problems {550}.

More details

Following renovation activities in a building in Egypt, Ulocladium was identified as a minor fungal type associated with suspended dust, representing 0.4% of the total count {1790}.

In a historic building, where occupants reported persistent health-related symptoms associated with sick-building syndrome, many fungi were found growing on building materials dampened by condensation {807}. These fungi had dispersed throughout the building in which many airborne fungi were identified, including Ulocladium sp. as a minor airborne contaminant.

A similar situation was reported in Argentina where researchers investigated the various types and concentrations of airborne fungi spores in 49 houses: although Ulocladium was among the thirteen dominant genera, it represented only 0.57% of the total fungal flora {1584}.

Laboratory section

Normal laboratory precautions should be exercised in handling cultures of this species within Biosafety Level 2 practices and containment facilities.

Colony, macroscopic morphology

Colonies are generally rapid growing, brown to olivaceous-black or greyish, with a suede-like to floccose texture; colonies mature within 5 days at 25°C {412}; on malt extract agar (MEA), they reach a diameter of 5.5 cm within 7 days at 25°C {724}.

On potato dextrose agar (PDA), colonies of Ulocladium grow rapidly with a woolly to cottony texture. The surface of the colonies is dark brown to olivaceous black; the reverse is black {2207; 725; 3283; 415}. 

Ulocladium chartarum colonies resemble those of Alternaria alternata.

Microscopic morphology

The hyphae are septate and light to dark brown. Conidiophores are golden brown, simple or occasionally branched, 40-55 μm in length and 5-7 μm in diameter, smooth-walled, strongly geniculate (bent at points of conidial production), yielding a zigzag appearance. Conidia are typically dark brown, multicelled, obovoid (narrowest at the base) and often rough-walled.  

More details

The size of the conidia can vary from small (13-30 x 6-19 μm) to larger conidia (19-39 x 11-22 μm) depending on the species.  The conidia are brown to black, round to oval in shape, smooth walled or rough and verrucose. They are usually egg-shaped and have a narrower base compared to the apex. These conidia are typically muriform and have transverse and longitudinal septations. They are solitary (e.g. Ulocladium botrytis) or, more commonly, in short chains (e.g.Ulocladium chartarum). When chains are produced, a tubular, short outgrowth (short secondary conidiophores) is formed on the conidia at the point of secondary conidium formation {1836; 724; 415}.

Ulocladium chartarum is typical of the genus. Its conidiophores are erect, straight or flexuose, often somewhat geniculate;  they are mostly unbranched, up to 50 x 4-5 μm, golden brown and smooth-walled. Conidial scars are brown. Conidia are commonly in chains of 2-10, ellipsoidal or obovoidal, often with short beaks, medium brown to olivaceous, ultimately becoming black, verrucose, 18-38 x 11-20 μm, with 1-5 (commonly 3) transverse and several oblique or longitudinal septa. Secondary conidiophores are often present on the conidia. 
Conidia (dictyoconidia) are formed through a pore (poroconidia) by a sympodially elongating geniculate conidiophore and are usually solitary {3971}.

U. chartarum differs from U. botrytis by the presence of conidia frequently in chains and dark conidiophore scars. It is distinct from Alternaria alternata by having conidia which are coarsely verrucose as well as a short, spindle-shaped apex.

Note: Ulocladium species are often misidentified as Alternaria, being very similar to Alternaria alternata {1834}. The morphological basis for separating the genera is based on the (shape, form) of the conidia {1831}, which are obovoid with tapered and narrow bases, and with no or very short apical beaks {1831; 724; 415}. Ulocladium sp. and Alternaria sp. also differ in their antifungal susceptibilities {1835}.

Specific metabolites

Organics compounds (including VOCs)

The specific mVOC profile of Ulocladium is not known.

There are no published articles regarding to complete metabolite profile of Ulocladium on building materials.  One study has reported results relative to metabolites produced by Ulocladium botritys grown on three different building materials (pinewood, particle board and gypsum board); it was shown to produce a number of different VOCs (hydrocarbons, alcohols, ketones, esters, terpenes, etc.). However, because Ulocladium was grown mixed with four other fungi, no specific compounds could be attributed solely to Ulocladium {594}.

More details

The genus Ulocladium contains species with a potential as enzyme producers and bio-control agents. For example,Ulocladium produces interesting compounds that limit Botrytis infestations in growing crops.

In the indoor environment of damp buildings, many organic compounds, including microbial volatile organic compounds (mVOCs), have been identified associated with several fungal species. Some of these compounds are common to most fungal species and probably contribute to various health problems associated with indoor air quality. However many of the fungal metabolites identified are non reactive and are in low concentrations in indoor air {594}.

Mycotoxins

There are no reported mycotoxins produced by Ulocladium that would be deleterious to humans or animals. Ulocladiummetabolites (unnamed), found in house dust, were studied in vitro and demonstrated to possess ciliostatic properties {550}.

Ulocladium spp. produce certain toxic substances that are biologically active against other fungi and plant cells.

More details

Certain phytotoxic secondary metabolites of Ulocladium chartarum have been identified, such as ulocladols A and B which are new phytotoxins of terpenoid nature {4276}. These new exometabolites are of a mixed sesquiterpenoid-polyketide nature; they are structurally close to the host-specific toxins of Alternaria citri. Both substances inhibit the growth of cotton seeds.

Adverse health reactions

This fungus is rarely pathogenic for humans; few cases of opportunistic infections have been reported although this fungus is known to be allergenic. Ulocladium sp. is of low pathogenicity, and is very seldom reported as a human pathogen {1835}.

Irritation and inflammation

It is generally accepted that many fungal structural components, common to all moulds, can induce irritation and inflammation.

No particular irritation or inflammation symptoms have been attributed specifically to Ulocladium sp.

Allergic reactions

Ulocladium sp. is considered common to indoor and outdoor environments and is reported to cause allergic reactions in some people  {460; 4079; 3840; 3912}. Together with Alternaria and Stemphylium, it is considered by some authors as one of the most common mould allergens in the United States {808}.

Although Ulocladium is reported to contribute to the allergenic burden of fungi-sensitive individuals {725}, no specific data or information has been found concerning sensitivity prevalence. U. chartarum is related to Alternaria and there could be some cross-reactivity in subjects sensitized to Alternaria. Conversely, some positive results to Ulocladium allergic tests could be the result of cross reactions with Alternaria sensitisation. 

Allergic components and mechanism

Specific allergenic components of Ulocladium have only been scarcely studied in humans. However, one experimental study has established that allergen extracts of U. chartarum (Ulo c 1) are related in nature to Alt a 1, e.g. similar to those ofAlternaria alternata (Hong sg,2005): the same is said of other fractions (Ulo a 1, Ulo at 1, Ulo b 1, Ulo cu 1) from otherUlocladium species.

An experimental allergen fraction of Ulocladium botrytis, named Ulo b 1, has been registered with UNIPROT: this protein is also similar to Alt a 1, and may cause an allergic reaction in humans in addition to binding to IgE {3318}.

Hypersensitivity pneumonitis

No case of hypersensitivity pneumonitis associated to Ulocladium spp. has been reported.

Toxic effects (mycotoxicosis)

No human or animal mycotoxicosis associated to Ulocladium has been reported.

Infections and colonisations

This fungus is rarely associated with infections in humans; Ulocladium is not reported as an emerging opportunistic pathogen {1835}. It has been reported in some cases of subcutaneous, cutaneous and nail infections, mostly in immunocompromised subjects {3995}.

One case of extended infection of subcutaneous tissues occurred in a patient with underlying Brill-Symmer's disease and who had received corticosteroid therapy {1844}.

More details

An unusual case of Ulocladium atrum keratitis has been reported in Australia in a 43 year-old man without ocular injury or irritation; response to topical antifungal was rapid {1831}.

Moreover, species of this fungus were isolated from several cutaneous infections in immunocompromised patients {1831}, including U. chartarum {1834}. A cutaneous mycosis caused by U. chartarum was reported in a heart transplant recipient {1835}.

A Turkish study of non-dermatophytic filamentous fungi causing onychomycosis has shown that, in that country,Ulocladium was among the most frequently isolated genera, being the fourth with a frequency of 12% {1833}. In Italy, Romano et al. reported a case of onychomycosis caused by U. botrytis, occurring in a toe of a 45 year-old man {1834}. 

Ulocladium has also been recovered from other cases of onychomycosis. It is however worthwhile to note that some reported cases of infections caused by U. chartarum were initially erroneously classified as alternariosis {1834}.

Virulence factors

No particular virulence factors have been reported for Ulocladium spp. 

Specific settings

Nosocomial infections

No nosocomial infections due to Ulocladium have been reported.

No outbreaks due to exposure to Ulocladium sp.have been reported in the hospital setting.

More details

Ulocladium has been found in the hospital environment in high risk care units {1842; 1839}. Hence, even thoughUlocladium has been found in low concentrations in the hospital setting, this fungus could represent an opportunistic infection risk for immunocompromised patients {1842}.

Occupational diseases

No occupational infections due to Ulocladium have been reported.

No particular outbreaks due to exposure to Ulocladium sp.have been reported in the workplace.

More details

However, some species of Ulocladium (namely U. atrum and U. oudemansii) could eventually be used in the biocontrol of foliar diseases in horticulture:  thus it would be important to assess human exposure when used in certain agricultural practices {1830}.

Diagnostic tools

Cultures

There are currently no available data regarding the diagnostic value of cultivation of clinical specimens.

Histopathology

Examination of tissue sections of deep sited Ulocladium infections may reveal pale pigmented, ellipsoidal elements, similar to those seen in Alternaria infections {3977}.

Immunodiagnosis

Ulocladium chartarum allergen extracts are available commercially and specific testing may be useful in the diagnosis ofUlocladium sensitisation {808}. U. chartarum is genetically related to Alternaria and there is some cross-reactivity in the immune responses to these two allergens. 

No Ulocladium allergen or antigen are registered with the «Biological Products Deviation Reporting»  surveillance program of the Federal Drug Administration (FDA, 2008 register) {3285}.

Test IgE IgG Antigens Other
Skin Tests        
RAST-IgE X      
RAST-IgG        
ELISA-ELIFA        
Immunodiffusion        
Immunofluorescence        
Complement fixation        
PCR        
Other        

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