INTRODUCTION TO THE ENTOMOPHTHOROMYCOTA

Humber (2012) defined this group of former ‘Zygomycota’ as a basal collection of conjugating fungi. Though some of them are free-living soil saprobes, most are parasites of arthropods (insects and mites). Other taxa parasitized by members of this group include desmids, fern gametophytes, nematodes, and vertebrates. In general, they are filamentous and siphonaceous, but some are yeasts and many are cellular (filaments of cells separated by crosswalls). They form zygospores that are characteristically thick-walled, and they tend to be homothallic. Many do not undergo gametangial fusion (the form of conjugation that occurs in the former Zygomycota), but form azygospores, ‘sexual’ spores that develop without gametangial fusion. Asexual reproduction is through the production of conidia that are forcibly-ejected. The conidia are covered with a sticky substance that assures they adhere to particular targets. If the conidia do not land on an appropriate target, they germinate and form secondary conidia. Most taxa in this phylum are grouped according to the types of conidia.

Entomophthora (Figures 1 and 2) is a very good example of many taxa in this phylum. They typically attack and feed on insects, and E. muscae, in particular, feeds on flies. The infection begins (see Figure 2) when a conidiospore adheres to the fly’s abdomen. There, it germinates and penetrates the exoskeleton. Inside, the hyphae elaborate through the haemolymph, consuming it. In its last dying act (likely induced by the fungus), the fly climbs to a high point where it mummifies as conidia emerge from the thin chitinous joints between the abdominal segments and cause a rain of infective spores, some of which likely will encounter other victims. Because this taxon feeds on flies, it has been evaluated as a potential biological control for flies (Wolken et al. 2003).

Basidiobolus (Figure 3) is distinctive in that it has very large nuclei that are oval in form and often more than 10μm long. Τhe hyphae are septatate with individual cells having a single nucleus. Members of this genus cause zygomycosis in our species. The infection is manifest as hard, subcutaneous masses. In extreme cases, the fungus can invade heart tissue, etc., especially in immunocompromised individuals. It causes similar diseases in horses, cutaneous lesions in amphibians, and gastric lesions in dogs. They accomplish asexual reproduction by the forcible discharge of conidia, and they produce typical sexual zygospores. Free-living taxa can be found in soil and dung.

FIGURE 1. The carcass of a fly that had been infected with Entomophthora has masses of conidia emerging from between its segments. Image from http://www.uoguelph.ca/~gbarron/MISCELLANEOUS/ento2.htm

FIGURE 2. Life Cycle of Entomophthora. 1. Overwintering pupa of the cabbage root fly 2. Infective conidia of E. muscae 3. Infection of adult fly 4. Conidiophores emerging from fly carcass 5. Discharged conidia which infect other adult flies 6. Adult fly carcass with overwintering resting spores (zygospores) 7. Thick-walled zygospores in the soil image from Wolken et al. (2003)

FIGURE 3. Sporangia (text with tooltip) Sporangia are spore-bearing structures. of Basidiobolus. Image from http://www.mycology.adelaide.edu.au/gallery/photos/basidiobolus05.html

SYSTEMATICS OF THE ENTOMOPHTHOROMYCOTA

The zygospore-producing fungi, formerly placed in the phylum Zygomycota, are basal groups, and, like many other basal groups with diversity in form and taxa, are paraphyletic. Indeed, the main defining synapomorphy, the zygospore, appears to be primitive in the fungi that do not produce motile cells. This was one of the results of Lutzoni et al. (2004) in their comprehensive systematic study of the Fungi. Increasingly, molecular work has confirmed that the Zygomycota is not monophyletic. Schussler et al. (2001) removed the arbuscular mycorrhizal (AM) fungi from the Zygomycota and defined them as a separate phylum, the Glomeromycota. Lutzoni et al. (2004) in a SSU and LSU r-RNA study of the Kingdom Fungi show that the existing orders of Zygomycota occupy at least 4 different monophyletic lines. Also, White et al. (2006), in an analysis of the r-RNA operon, confirm the paraphyletic nature of the traditional groups of Zygomycota. In their analysis, the zygomycotes could be divided into three independent clades, Thus, the group could be fragmented into at least three (White et al. 2006) or four (Lutzoni et al. 2004) more phyla. The organization of the conjugating fungi in our system is an interpretation of White et al. (2006) and Lutzoni et al. (2004), but informed by Tanabe et al. (2006) and Hibbett et al. (2007) and separates the former Zygomycota into the following higher taxa: Mucoromycota, Glomeromycota, Entomophthoromycota, and Kickxiellomycota.

The zygospore-producing fungi are taxa that superficially resemble some of the conjugating algae. They clearly are fungi in which the the dikaryotic phase does not go beyond the bounds of the zygospore. For many taxa, the vegetative filaments do not have septa and are haploid. Bruns et al. (1992) in their examination of 18S rRNA nucleotide sequences, confirmed that the chytrids and the conjugating fungi were basal groups within the clade of the Kingdom Fungi. Mainly, the conjugating fungi, like the rest of the fungi, never produce flagella at any stage in their life history. More recently, further molecular evidence (see Tudge, 2000 and Patterson, 1999 for a synopsis) has confirmed their position near the root of the fungi [see also Lang, The Fungal Mitochondrial Genome Project], which is part of a larger clade called the opisthokonts, a group that includes the choanoflagellates and the metazoans (Patterson, 1999). Margulis and Schwartz (1998) still maintain that the fungi are a kingdom of conjugating taxa, and, therefore, include the zygomycota.

The Entomophthoromycota as a phylum was defined by Humber (2012) and confirmed by Gryzanskyi et al. (2013, see Figure 4). Humber (2012) organizes the phylum into three classes: Basidiobolomycetes, Neozygitomycetes, and Entomophthoromycetes. Tanabe et al. (2005), however, were unable to resolve a monophyletic relationship of the classes and found that Basidiobilobus emerges as a very basal taxon that is sister to the Blastocladiomycota. Basidiobilobus, in Tanabe et al. (2004) emerged within the Kickxiellomycota. Humber (2012) acknowledged the problems with Basidiobilobus, but stressed that the similarities in structure and life history unite them with other members of the Entomophthoromycota. Gryzanskyi et al. (2013) suggest that the Entomophthoromycota might be oldest extant lineage of non-flagellated fungi and may be the closest relative of the Microsporidia.