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B. ranarum - Overview
Taxonomy & Phylogeny:
Basidiobolus ranarum was first described from a frog isolate in 1886 by Eidam. As a fungal species, B. ranarum is not known to have any common names, although synonymy has been considerable throughout the ages. Previously, the names Basidiobolus haptosporus Drechsler, Basidiobolus haptosporus var. haptosporus Drechsler, Basidiobolus haptosporus var. meristosporus (Drechsler) Srinivasan & Thirumalachar, Basidiobolus haptosporus var. minor Srinivasan & Thirumalachar, Basidiobolus heterosporus Srinivasan & Thirumalachar, and Basidiobolus meristosporus Drechsler were used (“Species Synonomy,” n.d.).
Molecular data can be found in Genbank. As of 11/4/2016, there were 130 matches to B. ranarum: 82 nucleotide and 48 protein sequences (https://www.ncbi.nlm.nih.gov/gquery/?term=basidiobolus+ranarum).
In culture, yellow-cream colonies initially appear flat, waxy, and glabrous; however, as growth radiates outward, folds appear and the white, aseptate mycelia dust the surface, giving the colony a powered appearance (“Basidiobolus ranarum,” n.d.). The overlaid mycelia causes a slight change in color from yellow-cream to cream-grey.
Microscopic examination reveals characteristic, “beaked” zygospores formed from relatively large (8-20 pm in diameter) vegetative hyphae; “appressed beak-like appendages” bookshelf the thick-walled, globose zygospores (Gugnani, 1999). These unique zygospores are a hallmark of the genus Basidiobolus and are useful for identification purposes, as their clinically-significant relatives (i.e., Canidiobolus species) lack these beaked zygospores. Additionally, both primary and secondary conidia can be viewed. Primary conidia are globose, much like the zygospores, but lack beaked appendages; secondary or replicative conidia are club-shaped (“Basidiobolus ranarum,” n.d). The discharge of both primary and secondary conidia takes place via a conidiophore: primary conidia are actively discharged from swollen cells while secondary conidia are released passively from the tips (Gugnani, 1999). In culture, the actively-discharged conidia will coat the lid of Petri dishes (Weber and Webster, 1998).
Colony growth is moderately fast at 30C, and overall growth is greatly enhanced by conidial germination. Upon forcible discharge, primary conidia form satellite colonies that surround the center, primary colony (“Basidiobolus ranarum,” n.d.).
Ecology & Biology:
Basidiobolus ranarum is found on every continent, in or on a myriad of materials and organisms. The fungi is transported by insects that are then eaten by insectivorous reptiles and amphibians (Webster, 1980; Alexopoulos et al., 1996). B. ranarum is thought to be part of the normal gut flora of many animals (Okafor et al., 1984) and has also been isolated from soil samples and decaying plants (Hospenthal and Rinaldi, 273).
The role that B. ranarum plays depends on the environment in which it is found. It exists as a saprophyte and feeds on dead plants, soil, and animal dung. Its spores readily persist within the environment, and it is in this form that B. ranarum likely internalized. Animals can acquire the fungus by long-term exposure, inhaling spores, drinking infected water, or feeding on infected plant material (Greene et al., 2002). Generally speaking, the fungi is not harmful when ingested; rather, it acts as an internal symbiont and simply becomes part of the animals’ “endogenous microflora” (Greene, 2002).
Under certain conditions, however, B. ranarum can cause significant damage. Despite its nearly ubiquitous presence throughout the globe, it is only sporadically pathogenic and scarcely known. Very rarely, gastrointestinal infection occurs and has been reported in humans (Joe and Njo-Imjo, 1956) horses (Owen et al., 1984), and dogs (Greene, 2002).
Relevance & Human Disease:
Human disease caused by B. ranarum is manifested subcutaneously or gastrointestinally, and it is thought to be restricted to tropical and subtropical areas of Africa, Asia, South America (Anand, 2010) and Australia (“Basidiobolus ranarum,” n.d.).
Traditionally, skin infections caused by B. ranarum have been referred to as subcutaneous zygomycosis (given the former placement of B. ranarum within Zygomycota), but entomophthoromycosis basidiobolae, subcutaneous phycomycosis, and basidiobolomycosis are synonymous (Gugnani, 1999). Subcutaneous lesions appear which then progress in form from small nodules to large, painless, subcutaneous granulomas (“Zygomycosis,” n.d.). Infection occurs most often on the perianum, limbs, chest, or back, and occurs primarily on adolescent males (Clark, 1968; Verma et al., 2012). While the mode of transmission is unknown, subcutaneous infection is thought to occur in one of two ways: 1) fungi is vectored by biting insects (Gugnani, 1999), or 2) using decaying leaves as toilet paper (Clark, 1968). The hypothesized reason for the male-skewed distribution is likely due to the latter.
As mentioned, B. ranarum is also capable of causing gastrointestinal infection; however, this is exceedingly rare. The first of such human infection (“entomophthoromycosis,” now called “basidiobolomycosis”) was diagnosed in an Indonesian patient in 1956 (Joe and Njo-Imjo).
Two important pathogenic relatives within the phylum Glomeromyctoa, order Entomophthorales are Conidiobolus coronatus and C. incongruous (Gugnani, 1999). Both species can cause similar disease, although subcutaneous zygomycosis caused by Conidiobolus generally afflicts the nasofacial region, and the infection itself is known by a different name: conidiobolomycosis (Hospenthal and Rinaldi, 272).
Histologically, the use of immune-florescent techniques, KOH, and H & E stains are helpful in the identification of B. ranarum from lesion biopsies. By tagging fungus-specific antibodies with fluorescein dye, the broad, vegetative hyphae can be visualized (Kwon-Chung 1992). H & E stains can also be used to manifest the Splendore-Hoeppli phenomenon: “thick, eosinophilic, hyalinized sheath[s] surrounding… thin-walled fungal hyphae” (de Souza Vianna, 2005). A combination of histological tests should be used to reach a comprehensive diagnosis.
Once a confident diagnosis has been reached using the above procedures, treatment can ensue via surgical intervention and/or the use of fungicides such as potassium iodide (Taylor, 1987). For best results, it is oftentimes necessary to simultaneously employ the aforementioned options with hyperbaric oxygen treatments (Ribes, 2000).