Microsporidia

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Microsporidia
Fibrillanosema spore.jpg
Sporoblast of
Fibrillanosema crangonycis
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Amorphea
Clade: Obazoa
(unranked): Opisthokonta
Clade: Holomycota
Kingdom: Fungi
Subkingdom: Rozellomyceta
Class: Microsporidiomycota
Benny 2007
Classes & orders [1]
Synonyms
  • Microsporidia Balbiani, 1882 [2]
  • Microsporidiida Labbé, 1899
  • Cnidosporidia Doflein 190?
  • Microsporea Delphy, 1936 [1963], Levine et al., 1980 [3] [4]
  • Microsporidea Corliss & Levine 1963 [5]
  • Microspora Sprague, 1969, 1977 [6]
  • Microsporida Tuzet et al. 1971

Microsporidia are a group of spore-forming unicellular parasites. These spores contain an extrusion apparatus that has a coiled polar tube ending in an anchoring disc at the apical part of the spore. [7] They were once considered protozoans or protists, but are now known to be fungi, [8] or a sister group to true fungi. [9] These fungal microbes are obligate eukaryotic parasites that use a unique mechanism to infect host cells. [7] They have recently been discovered in a 2017 Cornell study to infect Coleoptera on a large scale. So far, about 1500 of the probably more than one million [10] species are named. Microsporidia are restricted to animal hosts, and all major groups of animals host microsporidia. Most infect insects, but they are also responsible for common diseases of crustaceans and fish. The named species of microsporidia usually infect one host species or a group of closely related taxa. Approximately 10 percent of the known species are parasites of vertebrates — several species, most of which are opportunistic, can infect humans, in whom they can cause microsporidiosis.

Contents

After infection they influence their hosts in various ways and all organs and tissues are invaded, though generally by different species of specialised microsporidia. Some species are lethal, and a few are used in biological control of insect pests. Parasitic castration, gigantism, or change of host sex are all potential effects of microsporidian parasitism (in insects). In the most advanced cases of parasitism the microsporidium rules the host cell completely and controls its metabolism and reproduction, forming a xenoma. [11]

Replication takes place within the host's cells, which are infected by means of unicellular spores. These vary from 1–40 μm, making them some of the smallest eukaryotes.[ citation needed ] Microsporidia that infect mammals are 1.0–4.0 μm. [12] They also have the smallest eukaryotic genomes.

The terms "microsporidium" (pl. "microsporidia") and "microsporidian" are used as vernacular names for members of the group. The name MicrosporidiumBalbiani, 1884 [13] is also used as a catchall genus for incertae sedis members. [14]

Xenoma on flatfish caused by Glugea stephani Glugea stephani.jpg
Xenoma on flatfish caused by Glugea stephani

Morphology

Dictyocoela diporeiae. A, meront and spore; B, spore wall; C, polar filament Parasite140027-fig5 Dictyocoela diporeiae Winters & Faisal, 2014 transmission electron micrographs.tif
Dictyocoela diporeiae. A, meront and spore; B, spore wall; C, polar filament

Microsporidia lack mitochondria, instead possessing mitosomes. They also lack motile structures, such as flagella.

Microsporidia produce highly resistant spores, capable of surviving outside their host for up to several years. Spore morphology is useful in distinguishing between different species. Spores of most species are oval or pyriform, but rod-shaped or spherical spores are not unusual. A few genera produce spores of unique shape for the genus.

The spore is protected by a wall, consisting of three layers:

In most cases there are two closely associated nuclei, forming a diplokaryon , but sometimes there is only one.
The anterior half of the spore contains a harpoon-like apparatus with a long, thread-like polar filament, which is coiled up in the posterior half of the spore. The anterior part of the polar filament is surrounded by a polaroplast, a lamella of membranes. Behind the polar filament, there is a posterior vacuole. [11]

Infection

In the gut of the host the spore germinates; it builds up osmotic pressure until its rigid wall ruptures at its thinnest point at the apex. The posterior vacuole swells, forcing the polar filament to rapidly eject the infectious content into the cytoplasm of the potential host. Simultaneously the material of the filament is rearranged to form a tube which functions as a hypodermic needle and penetrates the gut epithelium.

Once inside the host cell, a sporoplasm grows, dividing or forming a multinucleate plasmodium, before producing new spores. The life cycle varies considerably. Some have a simple asexual life cycle, [16] while others have a complex life cycle involving multiple hosts and both asexual and sexual reproduction. Different types of spores may be produced at different stages, probably with different functions including autoinfection (transmission within a single host).

Medical implications

In animals and humans, microsporidia often cause chronic, debilitating diseases rather than lethal infections. Effects on the host include reduced longevity, fertility, weight, and general vigor. Vertical transmission of microsporidia is frequently reported.

In the case of insect hosts, vertical transmission often occurs as transovarial transmission, where the microsporidian parasites pass from the ovaries of the female host into eggs and eventually multiply in the infected larvae. Amblyospora salinaria n. sp. which infects the mosquito Culex salinarius Coquillett, and Amblyospora californica which infects the mosquito Culex tarsalis Coquillett, provide typical examples of transovarial transmission of microsporidia. [17] [18] [19] [20] Microsporidia, specifically the mosquito-infecting Vavraia culicis , are being explored as a possible 'evolution-proof' malaria-control method. [21] Microsporidian infection of Anopheles gambiae (the principal vector of Plasmodium falciparum malaria) reduces malarial infection within the mosquito, and shortens the mosquito lifespan. [22] As the majority of malaria-infected mosquitoes naturally die before the malaria parasite is mature enough to transmit, any increase in mosquito mortality through microsporidian-infection may reduce malaria transmission to humans. In May 2020, researchers reported that Microsporidia MB, a symbiont in the midgut and ovaries of An. arabiensis , significantly impaired transmission of P. falciparum, had "no overt effect" on the fitness of host mosquitoes, and was transmitted vertically (through inheritance). [23]

Clinical

Microsporidian infections of humans sometimes cause a disease called microsporidiosis. At least 14 microsporidian species, spread across eight genera, have been recognized as human pathogens. These include Trachipleistophora hominis . [24]

As hyperparasites

A hyperparasitic microsporidian, Nosema podocotyloidis, a parasite of a digenean which is itself a parasite of a fish. Parasite140019-fig4 Nosema podocotyloidis - Hyperparasitic Microsporidia.tif
A hyperparasitic microsporidian, Nosema podocotyloidis, a parasite of a digenean which is itself a parasite of a fish.

Microsporidia can infect a variety of hosts, including hosts which are themselves parasites. In that case, the microsporidian species is a hyperparasite, i.e. a parasite of a parasite. As an example, more than eighteen species are known which parasitize digeneans (parasitic flatworms). These digeneans are themselves parasites in various vertebrates and molluscs. Eight of these species belong to the genus Nosema . [25] Similarly, the microsporidian species Toguebayea baccigeri is a parasite of a digenean, the faustulid Bacciger israelensis, itself an intestinal parasite of a marine fish, the bogue Boops boops (Teleostei, Sparidae). [26]

Genomes

Microsporidia have the smallest known (nuclear) eukaryotic genomes. The parasitic lifestyle of microsporidia has led to a loss of many mitochondrial and Golgi genes, and even their ribosomal RNAs are reduced in size compared with those of most eukaryotes. As a consequence, the genomes of microsporidia are much smaller than those of other eukaryotes. Currently known microsporidial genomes are 2.5 to 11.6 Mb in size, encoding from 1,848 to 3,266 proteins which is in the same range as many bacteria. [27]

Horizontal gene transfer (HGT) seems to have occurred many times in microsporidia. For instance, the genomes of Encephalitozoon romaleae and Trachipleistophora hominis contain genes that derive from animals and bacteria, and some even from fungi. [27]

DNA repair

The Rad9-Rad1-Hus1 protein complex (also known as the 9-1-1 complex) in eukaryotes is recruited to sites of DNA damage where it is considered to help trigger the checkpoint-signaling cascade. Genes that code for heterotrimeric 9-1-1 are present in microsporidia. [28] In addition to the 9-1-1 complex, other components of the DNA repair machinery are also present indicting that repair of DNA damage likely occurs in microsporidia. [28]

Phylogeny

Phylogeny of Rozellomycota [29] [30]

Rozellomyceta
Rozellomycota
Rozellomycetes

Rozellales

Microsporidiomycota
Morellosporales

Mitosporidiaceae

Morellosporaceae

Paramicrosporidiales

Paramicrosporidiaceae

Nucleophagales

Nucleophagaceae

Microsporidia
Metchnikovellea

Metchnikovellida

Microsporidea

Neopereziida

Ovavesiculida

Amblyosporida

Glugeida

Nosematida

Classification

The first described microsporidian genus, Nosema , was initially put by Nägeli in the fungal group Schizomycetes together with some bacteria and yeasts. [31] [32] For some time microsporidia were considered as very primitive eukaryotes, placed in the protozoan group Cnidospora. [5] Later, especially because of the lack of mitochondria, they were placed along with the other Protozoa such as diplomonads, parabasalids and archamoebae in the protozoan-group Archezoa. [33] More recent research has falsified this theory of early origin (for all of these). Instead, microsporidia are proposed to be highly developed and specialized organisms, which just dispensed functions that are needed no longer, because they are supplied by the host. [34] Furthermore, spore-forming organisms in general do have a complex system of reproduction, both sexual and asexual, which look far from primitive.

Since the mid-2000s microsporidia are placed within the Fungi or as a sister-group of the Fungi with a common ancestor. [35] [36] [37] [38]

Work to identify clades is largely based on habitat and host. Three classes of Microsporidia are proposed by Vossbrinck and Debrunner-Vossbrinck, based on the habitat: Aquasporidia, Marinosporidia and Terresporidia. [39]

A second classification by Cavalier-Smith 1993: [40]

Alimov 2007 [41] Wijayawardene et al. 2020 [29] [42]

See also

Related Research Articles

<i>Plasmodium</i> Genus of parasitic protists that can cause malaria

Plasmodium is a genus of unicellular eukaryotes that are obligate parasites of vertebrates and insects. The life cycles of Plasmodium species involve development in a blood-feeding insect host which then injects parasites into a vertebrate host during a blood meal. Parasites grow within a vertebrate body tissue before entering the bloodstream to infect red blood cells. The ensuing destruction of host red blood cells can result in malaria. During this infection, some parasites are picked up by a blood-feeding insect, continuing the life cycle.

<i>Wolbachia</i> Genus of bacteria in the Alphaproteobacteria class

Wolbachia is a genus of gram-negative bacteria that can either infect many species of arthropod as an intracellular parasite, or act as a mutualistic microbe in filarial nematodes. It is one of the most common parasitic microbes of arthropods, and is possibly the most common reproductive parasite in the biosphere. Its interactions with its hosts are often complex. Some host species cannot reproduce, or even survive, without Wolbachia colonisation. One study concluded that more than 16% of neotropical insect species carry bacteria of this genus, and as many as 25 to 70% of all insect species are estimated to be potential hosts.

Nosema apis is a microsporidian, a small, unicellular parasite recently reclassified as a fungus that mainly affects honey bees. It causes nosemosis, also called nosema, which is the most common and widespread of adult honey bee diseases. The dormant stage of N. apis is a long-lived spore which is resistant to temperature extremes and dehydration, and cannot be killed by freezing the contaminated comb. Nosemosis is a listed disease with the Office International des Epizooties (OIE).

<i>Plasmodium knowlesi</i> Species of single-celled organism

Plasmodium knowlesi is a parasite that causes malaria in humans and other primates. It is found throughout Southeast Asia, and is the most common cause of human malaria in Malaysia. Like other Plasmodium species, P. knowlesi has a life cycle that requires infection of both a mosquito and a warm-blooded host. While the natural warm-blooded hosts of P. knowlesi are likely various Old World monkeys, humans can be infected by P. knowlesi if they are fed upon by infected mosquitoes. P. knowlesi is a eukaryote in the phylum Apicomplexa, genus Plasmodium, and subgenus Plasmodium. It is most closely related to the human parasite Plasmodium vivax as well as other Plasmodium species that infect non-human primates.

Microsporidiosis is an opportunistic intestinal infection that causes diarrhea and wasting in immunocompromised individuals. It results from different species of microsporidia, a group of microbial (unicellular) fungi.

<i>Nosema</i> (microsporidian) Genus of parasitic fungi

Nosema is a genus of microsporidian parasites. The genus, circumscribed by Swiss botanist Carl Nägeli in 1857, contains 81 species. Most parasitise insects and other arthropods, and the best-known Nosema species parasitise honeybees, where they are considered a significant disease by beekeepers, often causing a colony to fail to thrive in the spring as they come out of their overwintering period. Eight species parasitize digeneans, a group of parasitic flatworms, and thus are hyperparasites, i.e., parasites of a parasite.

<span class="mw-page-title-main">Xenoma</span> Growth caused by various species of protists and fungi

A xenoma is a growth caused by various protists and fungi, most notably microsporidia. It can occur on numerous organisms; however is predominantly found on fish.

Paratransgenesis is a technique that attempts to eliminate a pathogen from vector populations through transgenesis of a symbiont of the vector. The goal of this technique is to control vector-borne diseases. The first step is to identify proteins that prevent the vector species from transmitting the pathogen. The genes coding for these proteins are then introduced into the symbiont, so that they can be expressed in the vector. The final step in the strategy is to introduce these transgenic symbionts into vector populations in the wild. One use of this technique is to prevent mortality for humans from insect-borne diseases. Preventive methods and current controls against vector-borne diseases depend on insecticides, even though some mosquito breeds may be resistant to them. There are other ways to fully eliminate them. “Paratransgenesis focuses on utilizing genetically modified insect symbionts to express molecules within the vector that are deleterious to pathogens they transmit.” The acidic bacteria Asaia symbionts are beneficial in the normal development of mosquito larvae; however, it is unknown what Asais symbionts do to adult mosquitoes.

Nosema ceranae is a microsporidian, a small, unicellular parasite that mainly affects Apis cerana, the Asiatic honey bee. Along with Nosema apis, it causes the disease nosemosis, the most widespread of the diseases of adult honey bees. N. ceranae can remain dormant as a long-lived spore which is resistant to temperature extremes and dehydration. This fungus has been shown to act in a synergistic fashion with diverse insecticides such as fipronil or neonicotinoids, by increasing the toxicity of pesticides for bees, leading to higher bee mortality. It may thus play an indirect role in colony collapse disorder. In addition, the interaction between fipronil and N. ceranae induces changes in male physiology leading to sterility.

Avian malaria is a parasitic disease of birds, caused by parasite species belonging to the genera Plasmodium and Hemoproteus. The disease is transmitted by a dipteran vector including mosquitoes in the case of Plasmodium parasites and biting midges for Hemoproteus. The range of symptoms and effects of the parasite on its bird hosts is very wide, from asymptomatic cases to drastic population declines due to the disease, as is the case of the Hawaiian honeycreepers. The diversity of parasites is large, as it is estimated that there are approximately as many parasites as there are species of hosts. As research on human malaria parasites became difficult, Dr. Ross studied avian malaria parasites. Co-speciation and host switching events have contributed to the broad range of hosts that these parasites can infect, causing avian malaria to be a widespread global disease, found everywhere except Antarctica.

<span class="mw-page-title-main">Nosematidae</span>

The Nosematidae are a family of microsporidians from the order Nosematida known for parasitizing insects.

Encephalitozoon intestinalis is a parasite. It can cause microsporidiosis.

<i>Encephalitozoon cuniculi</i> Microsporidial pathogen

Encephalitozoon cuniculi is a microsporidial parasite of mammals with world-wide distribution. An important cause of neurologic and renal disease in rabbits, E. cuniculi can also cause disease in immunocompromised people.

Nosema bombi is a microsporidian, a small, unicellular parasite recently reclassified as a fungus that mainly affects bumble bees. It was reclassified as Vairimorpha bombi in 2020. The parasite infects numerous Bombus spp. at variable rates, and has been found to have a range of deleterious effects on its hosts.

The microsporidian Cucumispora dikerogammari is a parasitic fungal species that infects the invasive amphipod Dikerogammarus villosus. The first recorded evidence of Cucumispora dikerogammari was, as cited by Ovcharenko and Vita, in Germany, circa 1895, by Dr. L. Pfeiffer in the Dnieper Estuary. The Dnieper Estuary and lower parts of the Danube River are considered to be the parasite’s native range. As its host, D. villosus, began to invade novel habitats, C. dikerogammari followed, and has now expanded its range to be found in many of the main bodies of water in Central and Western Europe. At this time, only limited research has been conducted regarding the ecological implications of C. dikerogammari spreading beyond its native range. However, there is evidence to suggest that C. dikerogammari may cause imbalance to the male/female sex ratio of its host D. villosus.

<i>Ordospora colligata</i> Intracellular parasite

Ordospora colligata is an intracellular parasite belonging to the Microsporidia. It is an obligatory gut parasite with the crustacean Daphnia magna as its only host. So far it has been reported from Europe and Asia.

<i>Hamiltosporidium</i> Genus of fungi

Hamiltosporidium is a genus of Microsporidia, which are intracellular and unicellular parasites. The genus, proposed by Haag et al. in 2010, contains two species; Hamiltosporidium tvaerminnensis, and Hamiltosporidium magnivora. Both species infect only the crustacean Daphnia magna (Waterflea).

Nematocida parisii is a parasitic species of Microsporidia fungi found in wild isolates of the common nematode, Caenorhabditis elegans. The fungus forms spores and replicates in the intestines before leaving the host.

<i>Enterospora nucleophila</i> Species of parasitic protist

Enterospora nucleophila is a microsporidian infecting the gilt-head bream. It develops primarily within the nuclei of rodlet cells and enterocytes, at the intestinal epithelium. It can also be found in cytoplasmic position within other cell types, including phagocytes, at subepithelial layers. It is the causative agent of emaciative microsporidiosis of gilthead sea bream, a chronic condition manifested as a severe growth arrestment, normally accompanied by trickling mortality.

Hazardia is a genus of microsporidians that parasite insects, with the type host being Culex pipiens. It is currently classified as incertae sedis within the order Amblyosporida of phylum Rozellomycota.

References

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