Bacillidium sp., from Nilsen (1999).

Belongs within: Opisthosporidia.
Contains: Marinosporidia, Terresporidia.

Polar parasites
Published 8 July 2023

Life as a parasite comes with its challenges but there has never been a shortage of those willing to have their sustenance provided by others. Among the spectrum of eukaryotes, none have committed more to the parasitic lifestyle than the microsporidians.

Spores of an unidentified microsporidian from an ocular infection, from the Center for Disease Control.

Microsporidians are obligate intracellular parasites that are renowned for including species with the smallest known genomes of any eukaryote. They also lack a number of the organelles of free-living eukaryotes, most notably mitochondria. Their level of genetic separation from other micro-organisms is such that they were once thought among the earliest-diverging of all eukaryotes. As phylogenetic methods improved, it was realised that the rudimentary nature of microsporidians was the result of secondary losses. Current opinion aligns the Microsporidia with fungi; whether the microsporidians are properly regarded as early-diverging fungi, or as part of the sister group of fungi, is largely a matter of where exactly one draws the line.

The majority of microsporidians may be placed within a clade that has been labelled Microsporida (Canning 1990) or Microsporea (Cavalier-Smith 1998). The primary characteristic uniting this clade is the polaroplast, a unique organelle within the microsporidian spore. The polaroplast is associated with the polar tube or polar filament, a tubular organelle that lies coiled within one end of the spore during dispersal (microsporidians outside the Microsporida clade also possess a polar tube but it is more rudimentary and lacks the associated polaroplast). When the spore comes in contact with a suitable host cell, swelling of the polaroplast fires the tube through the cell membrane. The infective sporoplasm is then injected through the polar tube directly into the host cell cytoplasm where it develops into the growing meront stage. By entering the host cell in this way, the new-born microsporidian is able to avoid many of the host’s immune responses.

Generalised internal structure of a microsporidan spore, from Keeling & Fast (2002).

As the microsporidian meronts grow and presumably multiply in the host cell, they may remain contained directly within the host cytoplasm or a vacuole may form about them. Without mitochondria, the meronts are entirely dependent on the host cell for the most basic elements of nutrition such as ATP. Different taxa may vary widely in their impact on the host, from minimal to mortal. In some cases, infection with microsporidians may induce the host cell itself to expand to gigantic size at the expense of surrounding cells, forming a cancer-like tumour called a xenoma.

Eventually, meronts will begin the process of forming spores. In some cases, this is as simple as laying down a protective coat of electron-dense material in the outer membrane, forming a single spore lying free in the host cytoplasm. In others, a vesicle forms around the developing sporont within which the parasite multiplies and divides to form a packet of multiple spores. Fusion of microsporidian cells and meiosis may occur as part of the process. Spores may also differ in the number of nuclei: some contain a single nucleus, others contain two nuclei in a close association known as a diplokaryon. Release of mature spores into the environment seems to be essentially passive, following the death and breakdown of the host cell.

Xenoma on a dab Limanda limanda, induced by the microsporidian Glugea stephani, copyright Hans Hillewaert.

Well over a thousand species of microsporidian have been described to date but the actual number in existence is undoubtedly much larger. Few if any animal groups are immune to microsporidian infections, and most microsporidian species are selective in their hosts. Even other parasites such as flukes and tapeworms may have their attackers; little fleas have smaller fleas within their cells, in this case. Historically, attempts have been made to classify microsporidians on the basis of features such as their mode of spore formation but such systems have proved vulnerable to further study. In some cases, a single species of microsporidian may form widely different spore types depending on factors such as growth conditions or location within the host (Stentiford et al. 2013). Molecular studies have suggested division of the Microsporida between three major clades that have been called the Marinosporidia, Aquasporidia and Terresporidia (Vossbrinck et al. 2014). The names of the clades reflect the environment in which the hosts of each can usually be found—marine, freshwater and terrestrial, respectively—but each clade includes exceptions to the usual pattern.

Partial life cycle of Ameson pulvis from Stentiford et al. (2013), showing potential alternative spore forms.

Microsporidians most strongly impact humans via their impact on domestic and other economically significant animals. Two particular parasites of insects stand out: Nosema apis, which causes nosemosis in bees, and N. bombycis, which causes pébrine in silkworms. The latter is notorious for an outbreak in France and Italy in the mid-1800s that led to the collapse of silk production in Europe. Direct infection of humans themselves by microsporidians is of most concern in sufferers of AIDS and other immunosuppressive disorders. Nevertheless, the impact of microsporidians on humans is not invariably negative. The Amblysporidae are a family of microsporidians that infects mosquitoes, and research has been conducted on whether they can be used in biological control. Little fleas have smaller fleas, and the flea of my flea might be a flea I want to keep around.

Systematics of Microsporea
<==Microsporea [Disporea, Nosematida, Pleistophorea]
|--Chytridopsida [Chrytridiopsidea, Minisporea]VD-VW14
| | i. s.: BuxtehudiaC-S98
| |--ChytridiopsidaeBJ02
| | |--Chytridiopsis Schneid. 1884 [incl. Chytridioides Tregnoboff 1913]KC01
| | |--NapamichumBJ02
| | |--IntextaBJ02
| | `--SteinhausiaVD-VW14
| |--Hessea [Hessidae]VD-VW14
| `--Burkea [Burkeidae]VD-VW14
`--Microsporida [Apansporoblastina, Microsporididea, Pansporoblastina]VD-VW14
| i. s.: Pseudopleistophoridae [Pseudopleistophorinae]VD-VW14
| Duboscqia [Duboscquiidae]VD-VW14
| TelomyxidaeVD-VW14
| |--TelomyxaOV95
| `--IssiaOV95
| |--I. globuliferaOV95
| |--I. singulati Ovčarenko & Vima 1995OV95
| `--I. trichopterae [=Perezia trichopterae]OV95
| Tuzetia [Monosporidae, Tuzetiidae]VD-VW14
| GlugeaC-S98 [GlugeidaeVD-VW14]
| |--G. americanusC02
| |--G. anomalaVD-VW14
| |--G. atherinaeMV04
| |--G. danilewskyiD56
| |--G. heraldiK-M02b
| |--G. hertwigiK-M02a
| |--G. plecoglossiHH99
| `--G. stephaniMS98
|--+--Parathelohania anophelisVD-VW14
| `--+--+--+--Culicosporella lunataVD-VW14
| | | `--Hyalinocysta chapmaniVD-VW14
| | `--Amblyospora [Amblyosporidae]VD-VW14
| | |--A. californicaVD-VW14
| | `--A. connecticusVD-VW14
| `--+--Marssonella elegansVD-VW14
| `--+--+--Octosporea muscadomesticaeVD-VW14
| | `--+--Trichotuzetia guttataVD-VW14
| | `--Hazardia milleriVD-VW14
| `--+--+--Larssonia obtusaVD-VW14
| | `--Berwaldia schaefernaiVD-VW14
| `--+--Gurleya [Gurleyidae]VD-VW14
| | `--G. daphniaeVD-VW14
| `--+--Senoma globuliferaVD-VW14
| `--Binucleata daphniaeVD-VW14
`--+--+--Caudospora [Caudosporidae]VD-VW14
| | `--C. simuliiVD-VW14
| `--‘Amblyospora’ bracteataVD-VW14
`--+--+--Hamiltosporidium magnivoraVD-VW14
| `--Neoflabelliforma aurantiaeVD-VW14
`--+--‘Thelohania’ parastaciVD-VW14
`--+--+--Systenostrema albaVD-VW14
| `--+--Fibrillanosema crangonycisVD-VW14
| `--+--Tubulinosema kingi [=Nosema kingi]VD-VW14
| `--+--Anncaliia algeraeVD-VW14
| `--KneallhaziaVD-VW14
| |--K. carolinensaeVD-VW14
| `--K. solenopsae [=Thelohania solenopsae]VD-VW14
`--+--Janacekia debaisieuxiVD-VW14
`--+--+--Neoperezia chironomiVD-VW14
| `--Bryonosema plumatellaeVD-VW14
`--+--Pseudonosema cristatellae [=Nosema cristatellae]VD-VW14
| |--B. filiferumMV04
| `--B. vesiculoformisVD-VW14
`--Trichonosema pectinatellaVD-VW14

*Type species of generic name indicated


[BJ02] Becnel, J. J., A. Jeyaprakash, M. A. Hoy & A. Shapiro. 2002. Morphological and molecular characterization of a new microsporidian species from the predatory mite Metaseiulus occidentalis (Nesbitt) (Acari, Phytoseiidae). Journal of Invertebrate Pathology 79: 163–172.

Canning, E. U. 1990. Phylum Microspora. In: Margulis, L., J. O. Corliss, M. Melkonian & D. J. Chapman (eds) 1990. Handbook of Protoctista. The structure, cultivation, habitats and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. A guide to the algae, ciliates, foraminifera, sporozoa, water molds, slime molds and the other protoctists pp. 53–72. Jones & Bartlett Publishers: Boston.

[C02] Caruso, J. H. 2002. Goosefishes or monkfishes. Family Lophiidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 264–270. Smithsonian Institute Press: Washington.

[C-S98] Cavalier-Smith, T. 1998. A revised six-kingdom system of life. Biological Reviews 73: 203–266.

[D56] Dawes, B. 1956. The Trematoda with special reference to British and other European forms. University Press: Cambridge.

[HH99] Hasegawa, M., & T. Hashimoto. 1999. Phylogenetic position of amitochondriate protists in the evolution of eukaryotes. Biological Bulletin 196: 389–392.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[K-M02a] Klein-MacPhee, G. 2002a. Smelts. Family Osmeridae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 162–170. Smithsonian Institute Press: Washington.

[K-M02b] Klein-MacPhee, G. 2002b. Pipefishes and seahorses. Family Syngnathidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder’s Fishes of the Gulf of Maine 3rd ed. pp. 321–326. Smithsonian Institute Press: Washington.

[MS98] Margulis, L., & K. V. Schwartz. 1998. Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth 3rd ed. W. H. Freeman and Company: New York.

[MV04] Méténier, G., & C. P. Vivarès. 2004. Genomics of microbial parasites: the microsporidial paradigm. In: Hirt, R. P., & D. S. Horner (eds) Organelles, Genomes and Eukaryote Phylogeny: An evolutionary synthesis in the age of genomics pp. 207–236. CRC Press.

[OV95] Ovčarenko, N. A., & I. Vima. 1995. Issia singulati sp. n. (Microsporidia, Telomyxidae): a new species of Microsporidia from Chironomus singulatus Meigen larvae from Kiev’s water reservoir. Gidrobiologicheskii Zhurnal 31 (5): 78–83.

Stentiford, G. D., K. S. Bateman, S. W. Feist, E. Chambers & D. M. Stone. 2013. Plastic parasites: extreme dimorphism creates a taxonomic conundrum in the phylum Microsporidia. International Journal for Parasitology 43: 339–352.

[VD-VW14] Vossbrinck, C. R., B. A. Debrunner-Vossbrinck & L. M. Weiss. 2014. Phylogeny of the Microsporidia. In: L. M. Weiss, & J. J. Becnel (eds) Microsporidia: Pathogens of Opportunity pp. 203–220. John Wiley & Sons, Inc.

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