Taxonomy of fungi causing mucormycosis and entomophthoramycosis (zygomycosis) and nomenclature of the disease: molecular mycologic perspectives

Abstract

Molecular phylogenetic analysis confirmed the phylum Zygomycota to be polyphyletic, and the taxa conventionally classified in Zygomycota are now distributed among the new phylum Glomeromycota and 4 subphyla incertae sedis (uncertain placement). Because the nomenclature of the disease zygomycosis was based on the phylum Zygomycota (Zygomycetes) in which the etiologic agents had been classified, the new classification profoundly affects the name of the disease. Zygomycosis was originally described as a convenient and inclusive name for 2 clinicopathologically different diseases, mucormycosis caused by members of Mucorales and entomophthoramycosis caused by species in the order Entomophthorales of Zygomycota. Without revision of original definition, the name "zygomycosis," however, has more often been used as a synonym only for mucormycosis. This article reviews the progress and changes in taxonomy and nomenclature of Zygomycota and the disease zygomycosis. The article also reiterates the reasons why the classic names "mucormycosis" and "entomophthoramycosis" are more appropriate than "zygomycosis."

Figure 1.

Old (A) and a proposed new (B) classification schemes of the kingdom Fungi.

Figure 2.

Phylogeny of fungi determined on the basis of small subunit ribosomal RNA sequences. Thick lines delineate clades supported by bootstrap values >90%. “Zygomycota” do not form monophyletic clades [9]. The metric bar indicates number of substitutions per site.

Figure 3.

Phylogenetic tree provided by T. Y. James at the University of Michigan, Ann Arbor, which was based on unpublished results from the AFTOL (Assembling the Fungal Tree of Life) project [10]. Results are similar to those reported by James et al [5], but additional basal taxa are included.

Figure 4.

Morphology of conidia and zygospores (scale bar, 20 μm). A, Reproduction of a conidium in Basidiobolus ranarum. A conidium discharged onto a Petri dish cover germinated and produced a conidiophore bearing a single conidium. B, Primary conidia of Conidiobolus incongruus germinated to produce long hyphae bearing subglobose conidia [38]. C, Secondary conidium formation by replication in Conidiobolus coronatus. D, Zygospore of Basidiobolus ranarum, with a characteristic beak, is produced by the fusion of 2 adjacent hyphal cells. E, Sporangial structure of Rhizopus species showing the sporangiophore (S), apophysis (A), columella (C), and sporangiospores (SP). F, Sporangium of Lichtheimia (Absidia) corymbifera. G, Electron microscopy of Zygospore (ZS) of Rhizopus species produced between 2 suspensors (S) originating from hyphae of 2 sexually compatible strains (courtesy of Dr S. L. Flegler). Images in A and C–F are from Kwon-Chung and Bennett [33].

Figure 5.

A, Basidiobolus ranarum in hematoxylin-eosin–stained tissue section showing a cross-section of hyphae with sleeves of eosinophilic material. B, Hyphae in longitudinal section in the same tissue shown in A. C, Angioinvasion in mucormycosis. A pulmonary blood vessel occluded by hyphae of Cunninghamella bertholletiae stained with hematoxylin-eosin. D, Hyphae of Rhizopus species in tissue stained by hematoxylin-eosin. Note the lack of eosinophilic material around the hyphae. Images are reproduced from Kwon-Chung and Bennett [33] (scale bar, 10 μm).