Updates on the Taxonomy of Mucorales with an Emphasis on Clinically Important Taxa

Abstract

Fungi of the order Mucorales colonize all kinds of wet, organic materials and represent a permanent part of the human environment. They are economically important as fermenting agents of soybean products and producers of enzymes, but also as plant parasites and spoilage organisms. Several taxa cause life-threatening infections, predominantly in patients with impaired immunity. The order Mucorales has now been assigned to the phylum Mucoromycota and is comprised of 261 species in 55 genera. Of these accepted species, 38 have been reported to cause infections in humans, as a clinical entity known as mucormycosis. Due to molecular phylogenetic studies, the taxonomy of the order has changed widely during the last years. Characteristics such as homothallism, the shape of the suspensors, or the formation of sporangiola are shown to be not taxonomically relevant. Several genera including Absidia, Backusella, Circinella, Mucor, and Rhizomucor have been amended and their revisions are summarized in this review. Medically important species that have been affected by recent changes include Lichtheimia corymbifera, Mucor circinelloides, and Rhizopus microsporus. The species concept of Rhizopus arrhizus (syn. R. oryzae) is still a matter of debate. Currently, species identification of the Mucorales is best performed by sequencing of the internal transcribed spacer (ITS) region. Ecologically, the Mucorales represent a diverse group but for the majority of taxa, the ecological role and the geographic distribution remain unknown. Understanding the biology of these opportunistic fungal pathogens is a prerequisite for the prevention of infections, and, consequently, studies on the ecology of the Mucorales are urgently needed.

Keywords: Mucorales; pathogens, identification, ecology, Circinella, Lichtheimia, Mucor, Rhizomucor, Rhizopus; taxonomy.

Figure 1

Morphology of the Mucorales. (a) Zygospore with equal suspensors of Mucor endophyticus CBS 385.95; (b) azygospore of Mucor bainieri CBS 293.63; (c) zygospores with unequal suspensors of Mucor multiplex (syn. Zygorhynchus multiplex) CBS 110662; (d) top view on a young mycelium with transitorily recurved sporangiophores; (e) recurved sporangiophore and (f) columella of Backusella recurva CBS 318.52; (g) sporangium with circumscissile zone of dehiscence and (h) discharged sporangium of Pilaira anomla CBS 699.71; (i) sporangiola-bearing complex sporophore of Thamnidium elegans CBS 341.55; (j) circinate sporangiophore branches with columellae and detached sporangiospores of Circinella umbellata; (k) hyphae of Rhizopus microsporus in human lung tissue. Scale bars = 50 µm except of d = 500 µm.

Figure 2

Classification of zygomycete fungi including the Mucorales based on Spatafora et al. [12]. Bold printed taxa contain pathogenic species.

Figure 3

Morphology of the opportunistic members of the Mucorales. (a) Sporangiophore with sporangium and indistinct apophysis and (b) with columella and detached sporangiospores of Rhizopus arrhizus JMRC:NRZ:1217; (c) sympodially branched sporangiophore of Mucor circinelloides NRZ-2019-468; (d) sympodially branched sporangiophore of Mucor ramosissimus CBS 135.65; (e) sporangiophore with columellae and detached sporangiospores of Lichtheimia ramosa NRZ-2019-435; (f) sporangiophore with columellae and detached sporangiospores of Rhizomucor pusillus JMRC:NRZ:0496; (g,k) sporangiophores of Apophysomyces variabilis; (h) sporophore with sporangiola and columella at the place of the former sporangium of Thamnostylum lucknowense JMRC:SF:00845; (i) sporophore of Saksenaea sp.; (j) sporophore with merosporangia of Syncephalastrum racemosum CBS 302.65; (l) young sporangiophore of Actinomucor elegans CBS 111556; (m) sporophores with single-spored sporangiola of Cunninghamella bertholletiae. Scale bars = 50 µm.