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Validation of Malasseziaceae and Ceraceosoraceae (Exobasidiomycetes)

Authors:
  • Institute of Biodiversity and Ecosystem Research, Sofia, Bulgaria

Abstract

Names of two families in the Exobasidiomycetes, Malasseziaceae and Ceraceosoraceae, are validated.
MYCOTAXON
 

Validation of Malasseziaceae and Ceraceosoraceae
(Exobasidiomycetes)


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
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Abstract          

Key words
Introduction







Validation of two family names
Malasseziaceaefam. nov.

      
        
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         

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         
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           
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
  
          
            




Ceraceosoraceaefam. nov.


           

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
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Acknowledgements
 
         
         
         
       
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Literature cited

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        
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   
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             
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... Thus, to accommodate the genus Ceraceosorus, Begerow et al. (2006) added the novel order Ceraceosorales, assigned to the class Exobasidiomycetes. The family Ceraceosoraceae was subsequently described by Denchev and Moore (2009). ...
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The order Ceraceosorales (Ustilaginomycotina) currently includes the single genus Ceraceosorus, with one species, Ceraceosorus bombacis, parasitic on Bombax ceiba in India. The diversity, biogeography, evolution, and phylogenetic relationships of this order are still relatively unknown. Here, a second species of Ceraceosorus is described from West Africa as a novel species, Ceraceosorus africanus, infecting Bombax costatum in Benin, Ghana, and Togo. This species produces conspicuous fructifications, similar to corticioid basidiomata when mature, but sorus-like in early stages of ontogenetic development. The fructifications cover much of the leaf surface and resemble leaf blight. This contrasts with the inconspicuous fructifications of C. bombacis comprising small spots scattered over the lower leaf surface that resemble leaf spot. Both species of Ceraceosorus differ in several micromorphological traits, infect different host plant species in widely separated geographical areas, and are separated by a considerable genetic distance in 28S rDNA and RPB2 genes. The distinct corticioid fructification of C. africanus is a unique morphological trait within the Ustilaginomycotina. Molecular phylogenetic analyses of a single gene dataset (D1/D2 28S rDNA) supported the monophyly of the two Ceraceosorus species and the Ceraceosorales and their placement within the Ustilaginomycotina. Molecular phylogenetic analyses of a multigene dataset (18S/5.8S/28S rDNA/RPB2/TEF1) revealed Exobasidium rhododendri (Exobasidiales) as the closest relative of Ceraceosorus, both clustering together with Entyloma calendulae (Entylomatales), indicating affinities to the Exobasidiomycetes. This phylogenetic placement is in agreement with ultrastructural characteristics (presence of local interaction zone and interaction apparatus) reported for the Ceraceosorales, Entylomatales, and Exobasidiales.
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Ustilaginomycotina (Basidiomycota, Fungi) has been reclassified recently based on multiple gene sequence analyses. However, the phylogenetic placement of two yeast-like genera Malassezia and Moniliella in the subphylum remains unclear. Phylogenetic analyses using different algorithms based on the sequences of six genes, including the small subunit (18S) ribosomal DNA (rDNA), the large subunit (26S) rDNA D1/D2 domains, the internal transcribed spacer regions (ITS 1 and 2) including 5.8S rDNA, the two subunits of RNA polymerase II (RPB1 and RPB2) and the translation elongation factor 1-α (EF1-α), were performed to address their phylogenetic positions. Our analyses indicated that Malassezia and Moniliella represented two deeply rooted lineages within Ustilaginomycotina and have a sister relationship to both Ustilaginomycetes and Exobasidiomycetes. Those clades are described here as new classes, namely Moniliellomycetes with order Moniliellales, family Moniliellaceae, and genus Moniliella; and Malasseziomycetes with order Malasseziales, family Malasseziaceae, and genus Malassezia. Phenotypic differences support this classification suggesting widely different life styles among the mainly plant pathogenic Ustilaginomycotina.
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The genus Malassezia has been revised using morphology, ultrastructure, physiology and molecular biology. As a result the genus has been enlarged to include seven species comprising the three former taxa M. furfur, M. pachydermatis and M. sympodialis, and four new taxa M. globosa, M. obtusa, M. restricta and M. slooffiae. The descriptions of all the species include morphology of the colonies and of the cells, together with ultrastructural details. The physiological properties studied were the presence of catalase, the tolerance of 37 degrees C and the ability to utilize certain concentrations of Tween 20, 40, 60 and 80 as a source of lipid in a simple medium. Information is given for each of the taxa on mole% GC and also the rRNA sequence from the comparison previously described for the genus.
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The molecular systematics of 337 strains of basidiomycetous yeasts and yeast-like fungi, representing 230 species in 18 anamorphic and 24 teleomorphic genera, was determined by sequence analysis of the D1/D2 region of the large-subunit rDNA. The data were compared with published sequences of other basidiomycetous fungi. The results demonstrated that the yeast species and genera are phylogenetically distributed among the Microbotryum, Sporidiobolus, Agaricostilbum and Erythrobasidium clades of the Urediniomycetes; the Tremellales, Trichosporonales ord. nov., Filobasidiales and Cystofilobasidiales clades of the Hymenomycetes; and the Ustilaginales, Microstromatales and Malasseziales clades of the Ustilaginomycetes. Genera such as Bensingtonia, Cryptococcus, Rhodotorula and Sporobolomyces are polyphyletic, i.e. they occur in two or more clades. In contrast, other genera, e.g. Bullera, Cystofilobasidium, Fellomyces, Filobasidiella, Filobasidium, Kondoa, Kurtzmanomyces, Leucosporidium, Rhodosporidium, Sporidiobolus and Udeniomyces, are monophyletic. The majority of the species can be identified using D1/D2 analyses, although the internal transcribed spacer region is required to distinguish closely related species. The intergenic spacer region is recommended for additional differentiation of species and strains.
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Five isolates of a novel species of the yeast genus Malassezia were isolated from animals in Japan and Brazil. Phylogenetic trees based on the D1/D2 domains of the large-subunit (26S) rDNA sequences and nucleotide sequences of the internal transcribed spacer 1 region showed that the isolates were conspecific and belonged to the genus Malassezia. They were related closely to Malassezia dermatis and Malassezia sympodialis, but were clearly distinct from these two species and the other six species of Malassezia that have been reported, indicating that they should be classified as a novel species, Malassezia nana sp. nov. Morphologically and physiologically, M. nana resembles M. dermatis and M. sympodialis, but can be distinguished from these species by its inability to use Cremophor EL (Sigma) as the sole lipid source and to hydrolyse aesculin. The type strain of M. nana is NUSV 1003T (=CBS 9557T=JCM 12085T).
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Proliferobasidium and Ceraceosorus (Brachybasidiaceae, Brachybasidiales, Basidiomycetes) are described as new genera. Both cause leaf-spot diseases of vascular plants and are characterized by persistent thick-walled probasidia and bisterigmate metabasidia. They differ from Dicellomyces, the most closely related genus, in having indeterminate rather than determinate hymenial thickening and in lacking a fruiting body with extensive sterile tissue. Proliferobasidium is based on P. heliconiae, described as a new species on Heliconia bihai. It has intercellular hyphae and exhibits repeated percurrent proliferation of new basidia from within persistent probasidial walls. Ceraceosorus, with the type species Dicellomyces bombacis on Bombax ceiba, has intracellular hyphae and lacks percurrent proliferation of basidia. Ceraceosorus bombacis is presented as a new combination. Since they have features in common with Uredinales, Dacrymycetales, and corticioid Homobasidiomycetes, Ceraceosorus and Proliferobasidium may prove to be of considerable evolutionary interest.
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In order to integrate ustilaginomycetous anamorphs into the general phylogenetic system of Ustilaginomycetes, partial nuclear large subunit ribosomal DNA sequences of 56 teleomorphic and 19 anamorphic species of the Ustilaginomycetes were analysed. Maximum parsimony and neighbour joining confirm the new suprageneric system of Ustilaginomycetes and indicate that (i) the species of Pseudozyma represent anamorphs of Ustilaginales parasitizing grasses, (ii) Pseudozyma prolifica, the type of Pseudozyma, is very closely related to Ustilago maydis, (iii) Pseudozyma tsukubaënsis is probably synonymous with Ustilago spermophora, (iv) the species of Malassezia represent a group of its own within the Exobasidiomycetidae, (v) Tilletiopsis cremea, T. lilacina and T. washingtonensis belong to the Entylomatales and (vi) T. flava, T. fulvescens and T. minor are members of the Georgefischeriales. Like all Tilletiopsis species tested, T. albescens and T. pallescens are members of the Exobasidiomycetidae, but they cannot be ascribed to any of the known orders of this subclass. The description of the Malasseziales is emended.
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The phylogeny of Auriculoscypha anacardiicola, an associate of scale insects in India, is investigated using subcellular characters and MP and Bayesian analyses of combined nuLSU-rDNA, nuSSU-rDNA and 5.8S rDNA sequence data. It has simple septa with a pulley-wheel-shaped pore plug, which is diagnostic of phytoparasitic members of the Pucciniomycetes, and hyphal wall break on branching, a phenomenon unique to some simple septate heterobasidiomycetes. The septal ultrastructure of A. anacardiicola is similar to that of the genus Septobasidium. The close relationship to Septobasidium is also confirmed by rDNA sequence analyses. The polyphyletic nature of the order Platygloeales, noted in earlier studies, is evident from the present molecular analysis as well. The placement of Auriculoscypha in the Platygloeales can no longer be justified and both ultrastructural and molecular evidence strongly support the placement of Auriculoscypha in the Septobasidiales.
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The genus Malassezia contains three member species: Malassezia furfur and Malassezia sympodialis, both obligatory lipophilic, skin flora yeasts of humans, and Malassezia pachydermatis, a nonobligatory lipophilic, skin flora yeast of other warm-blooded animals. Several characteristics suggest the basidiomycetous nature of these yeasts, although a perfect stage has not been identified. Classically, these organisms are associated with superficial infections of the skin and associated structures, including pityriasis versicolor and folliculitis. Recently, however, they have been reported as agents of more invasive human diseases including deep-line catheter-associated sepsis. The latter infection occurs in patients, primarily infants, receiving parenteral nutrition (including lipid emulsions) through the catheter. The lipids presumably provide growth factors required for replication of the organisms. It is unclear how deep-line catheters become colonized with Malassezia spp. Skin colonization with M. furfur is common in infants hospitalized in neonatal intensive care units, whereas colonization of newborns hospitalized in well-baby nurseries and of older infants is rarely observed. Catheter colonization, which may occur without overt clinical symptoms, probably occurs secondary to skin colonization, with the organism gaining access either via the catheter insertion site on the skin or through the external catheter hub (connecting port). There is little information on the colonization of hospitalized patients by M. sympodialis or M. pachydermatis. Diagnosis of superficial infections is best made by microscopic examination of skin scrapings following KOH, calcofluor white, or histologic staining. Treatment of these infections involves the use of topical or oral antifungal agents, and it may be prolonged. Diagnosis of Malassezia catheter-associated sepsis requires detection of the organism in whole blood smears or in buffy coat smears of blood drawn through the infected catheter or isolation of the organism from catheter or peripheral blood or the catheter tip. Culture of M. furfur from blood is best achieved with Isolator tubes and plating onto a solid medium supplemented with a lipid source. Appropriate treatment of patients requires removal of the infected catheter with or without temporary stoppage of lipid emulsions; administration of antifungal therapeutic agents does not appear to be necessary. Because many patients who develop Malassezia catheter-associated sepsis have severe underlying illnesses, caution must be exercised in attributing all clinical deterioration to Malassezia infection. Our better understanding of how these organisms cause disease awaits the development of a useful typing scheme for epidemiologic studies and further studies on microbial virulence factors and the role of the immune response in pathogenesis.