Parasitology. Alan Gunn

(Heyworth 2017). Nevertheless, some microsporidia are undoubtedly zoonotic and infect both humans and other mammals and birds. Indeed, some commentators consider them to be extremely important emerging pathogens (Stentiford et al. 2019). This is particularly the case now that global food chains mean that foodstuffs are rapidly transported around the world.

      Initially designated as protozoa, subsequent molecular evidence indicated that microsporidia are fungi. Precisely where they fit within the taxonomy of fungi is uncertain although they show some resemblance to the zygomycetes. The zygomycetes also have relevance to parasitologists since they include genera such as Pilobolus that helps to spread the infective larvae of the lungworm Dictyocaulus viviparus (Doncaster 1981) and Entomophthora that have potential as biological control agents of insect vectors. However, the taxonomic status of the microsporidia is far from settled and Ruggiero et al. (2015) consider that the phylum Microspora belongs back within the kingdom Protista.

      As with Entamoeba histolytica, the microsporidia were once thought to have split off from other organisms at an early stage in their evolution because they did not appear to contain mitochondria. However, they too were subsequently found to contain genes with mitochondrial functions and mitosomes (putative relict mitochondria). They also have some of the smallest genome sizes and the fewest protein coding genes of all the eukaryotic organisms; in Encephalitozoon intestinalis the genome is only 2.3 megabases (Mb) in size although in Glugea atherinae, a fish parasite, it is almost ten times larger at ~20 Mb.

The spore is the only microsporidian life cycle stage capable of surviving in the external environment. Immediately above the spore’s plasma membrane are two protective layers, the first of these is the ‘endospore’ which contains chitin and is electron luscent when viewed with a transmission electron microscope and above this is the ‘exospore’ that contains glycoprotein and is electron dense, so it appears dark in transmission electron micrographs (Figure 4.11). The spore walls must provide excellent protection because in some species they can remain infective for over a year.

Figure 4.11 Transmission electron micrograph of a developing spore of the microsporidian Nosema helminthorum. The thick spore coat makes sectioning extremely difficult, and they often pull out from the sample. The coiled polar tube is clearly visible as a series of circles either side of the upper portion of the cell. For further details, see text.

      Microsporidia are normally transmitted horizontally when the host encounters the spores; humans usually become infected by ingesting or breathing in the spores. Vertical transmission has not yet been described in humans, but it occurs in some mammals by crossing the placenta or through infecting the eggs while they are still in the ovary in invertebrates. Transovarial transmission is common among endosymbiotic bacteria such as Wolbachia but very rare among protozoan parasites (Dunn et al. 2001). Like Wolbachia, some of the microsporidia species that are transmitted transovarially affect the sex rations of their hosts. For example, females of the amphipod Corophium volutator infected with microsporidia produce predominantly female offspring. They are also more fertile than uninfected females and this will further promote the spread of the parasite through the population (Mautner et al. 2007).

Microsporidian spores, like the other life cycle stages, usually contain either a single nucleus (monokaryon) or two adjacent nuclei (diplokaryon) that function as a single unit. The spores also contain a posterior vacuole, and a structure called the ‘polaroplast’ that probably derives from modified Golgi apparatus. In addition, there is a coiled polar tubule (polar filament) that attaches to the anterior end of the spore by an ‘anchoring disc complex’. The polar tube is hollow and unique to the Microsporidia but in terms of appearance and function it bears more than a passing resemblance to the nematocysts found in jellyfish (Cnidaria). When the spore receives the correct stimulation (presumably a combination of pH and chemical factors), the posterior vacuole and polaroplast absorb water and start to swell. Because the tough spore wall prevents it from expanding, the pressure within the spore starts to rise. Ultimately, the spore wall ruptures at the anterior end where the spore wall is thinnest, and the polar tubule shoots out through the break as if from a harpoon gun. The polar tubule can discharge with sufficient force to pierce the adjacent host cell or alternatively it may be subsequently ingested by receptor‐mediated endocytosis. At the same time, the pressure within the spore forces the nucleus and cytoplasm, now referred to as the ‘sporoplasm’ down the everting polar tubule and thence into the host cell. The spore ensures its proximity to a suitable host cell by binding onto host‐cell sulphated glycosaminoglycans (GAGs). In addition, the exospore and endospore both contain an adherence protein called ‘endospore protein 1’ (EnP1). Alternatively, the host cell may ingest whole spore, but infection still results from the discharge of the sporoplasm into the host cell cytoplasm.

      Once within the host cell cytoplasm, the sporoplasm differentiates into a ‘meront’ and undergoes a series of cycles of asexual reproduction called merogony, which results in the formation of numerous more meronts. In the cases of Entercytozoon and Nosema, the meronts remain in direct contact with the host cell cytoplasm, whilst in Encephalitozoon they are localized within a membrane‐bound parasitophorous vacuole of host cell origin. The meronts of both Nosema and Encephalitozoon divide by simple binary fission, but those of Enterocytozoon have a more complex development which produces multinucleate cells. After several cycles of merogony, the parasites start to produce spores by sporogony: the meront transforms into a sporont which produce sporoblasts that then mature into spores. The spores steadily accumulate in the host cell and may eventually fill it. When the host cell membrane eventually ruptures, the spores are released and may infect an adjacent cell or be released into the environment.

      In humans, microsporidia usually cause persistent or self‐limiting infections of the enterocytes lining the gastrointestinal tract. They can cause extensive damage to the mucosal surface of the intestine and symptoms therefore typically cause diarrhoea, abdominal pain, malabsorption and wasting. There are also records of them invading the eye and causing keratitis in both immunocompromised and immunocompetent individuals, as well as infecting the skin, kidney, heart, and lungs.