16.3 Trichomycetes

Microsporidia are fungi that were long thought to be protozoans, and are still called protozoans by many people who should know better. Trichomycetes, on the other hand, includes organisms that are clearly protozoans though they were mistakenly classified as fungi for a long time, and are still called fungi by many people who should know better.

These extremely common organisms live only in the digestive tracts of insects and other arthropods, generally as commensals, sometimes as pathogens or symbionts (mutualists), which are associated with, although not penetrating, the cuticle lining the digestive tracts of the host animal. Their hosts include terrestrial, marine and freshwater arthropods, most commonly midges (Chironomidae), mosquitoes (Culicidae), black flies (Simuliidae), beetles (Coleoptera), stoneflies (Plecoptera), and mayflies (Ephemeroptera), as well as several millipedes (Diplopoda) and crustaceans.

The traditional taxonomy is based on a few micromorphological characters and the traditional view was to place the class Trichomycetes in the Zygomycota, the class being divided into four orders:

  • Amoebidiales (which occur on the external surfaces of freshwater arthropods),
  • Asellariales,
  • Eccrinales, and
  • Harpellales.

See the section entitled The traditional Zygomycota in Chapter 3 for some discussion of the taxonomic placement of Harpellales and the polyphyletic nature of the taxon ‘Zygomycota’ (CLICK HERE to view the page now). Characteristically, the Trichomycetes develop nonseptate (in the Amoebidiales and Eccrinales) or irregularly septate (in the Harpellales and Asellariales) vegetative mycelia and asexual sporangia. Further, most genera of the Harpellales produce zygospores and it is this character which was used to include all the Trichomycetes in the Zygomycota. The Amoebidiales and the Eccrinales have now been removed from this association.

The Amoebidiales are amoebae-producing organisms that attach to the exoskeleton of freshwater arthropods (Amoebidium parasiticum was the first described). Production of amoebae is not otherwise present in kingdom Fungi. More significantly, A. parasiticum has stacked dictyosomes, which do not occur in fungi, and also lacks chitin in its cell wall. Taken together these features do not make it a good candidate as a fungus and eventually molecular phylogenetic analysis of relationships removed the order Amoebidiales from the Trichomycetes to the protozoan class Mesomycetozoea (Benny & O’Donnell, 2000).

The Eccrinales have unbranched, non-septate, multinucleate thalli, and produce sporangiospore, which form from the apex downward toward the base of the thallus, a feature found only in kingdom Fungi. These few distinctive morphological characters together with the fact that they share a very specialised ecological niche with genuine fungi like the Harpellales was all that classified them within the Trichomycetes. Now sequence analyses has showed that the Eccrinales share a common ancestry with the Amoebidiales, and now both orders are placed in the class Mesomycetozoea, which is positioned at the animal-fungi boundary in the opisthokont lineage (Mendoza, Taylor & Ajello, 2002; Cafaro, 2005).

Removing these fungus-like protozoans leaves the Trichomycetes consisting of the Harpellales and Asellariales. CLICK HERE to see a page of illustrations.

These are true fungi having hyphal thalli with cell walls containing chitin fibrils and being regularly septate with incomplete septa having a plugged central pore. No confirmed sexual stage has been reported generally for the Asellariales, although conjugation has been reported between cells of the one species Asellaria ligiae. Generally in the Harpellales, though, zygospores (biconical and apically thickened when mature, see Fig. 3) form following conjugation between cells of the same, or different thalli, being borne at the apex of zygosporophores.

Diagram of the general pattern of asexual reproduction in Smittium (Harpellales)
Fig. 3. Diagram of the general pattern of asexual reproduction in Smittium (Harpellales). Redrawn after Moss & Young, 1978.

Phylogenetic analyses confirm that these Trichomycetes (that is, the Harpellales and Asellariales) belong to the subphylum Kickxellomycotina within the traditional phylum Zygomycota (White, 2006; White et al., 2006), although this is a heterogeneous collection (see our earlier discussion in Chapter 3; CLICK HERE to view the page). A major difficulty for study of these organisms is that they are microfungi which are highly specialised for attachment to the gut wall of arthropods and they are obligate endosymbionts; consequently, very few of them can be cultured axenically (= in pure culture) although this is needed to prepare fungal macromolecules free of contaminating host molecules. Only eight of the 38 genera of Harpellales have been cultured, but none of the Asellariales.

The unique trichospores, for which the class is named, are the asexual spores. Harpellales produce branched or unbranched thalli, and either the entire thallus or lateral branches of it become regularly septate at maturity to form a series of uninucleate generative cells. From the apical region of each generative cell a single unisporous merosporangium is produced; this is the trichospore (Fig. 3). In many genera the merosporangia are borne on short lateral branches, which form the collar region of the generative cell. Members of the Asellariales do not produce deciduous merosporangia but the regularly septate branches fragment into single-celled arthrospores. In some species of Asellariales the arthrospores germinate by producing a single branch, similar in position and form to a trichospore.

These insect gut fungi occur worldwide in all habitats; effectively they have been found whenever they have been looked for. The Harpellales are predominantly associated with larval aquatic insects, and, occasionally, with freshwater isopod crustaceans, attached to the midgut or hindgut linings.

They also attach to the midgut linings of lower dipterans (Nematocera, which includes mosquitoes, crane flies, black flies, gnats and midges), mayflies (Ephemeroptera), stoneflies (Plecoptera), beetles (Coleoptera) and caddisflies (Trichoptera).

The Asellariales includes species that inhabit terrestrial, freshwater and marine isopods (Isopoda: Crustacea) such as woodlice, pill bugs, and sea slaters; as well as the hexapod springtails (Collembola) that are primitive relatives of insects.

They are most often described as being symbiotic with their hosts but the nature of the association is not at all clear. Certainly, the fungi are highly specialised for existence within the arthropod guts, so they may be commensals (an association in which one species derives some benefit while the other is unaffected). But as fungi they are able to produce many digestive enzymes so this may be a mutualistic symbiosis in which the fungus provides nutrients to the insect hosts by assisting with food digestion. A few species appear to be parasitic at some stage of the host’s development. All the evidence suggests that only a fraction of the species of arthropod gut fungi is known.

Updated December 17, 2016