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Category: Microbial Genetics and Molecular Biology; Environmental Microbiology
Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom, Page 1 of 2
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Microsporidia were initially described about 150 years ago with the identification of Nosema bombycis as the organism responsible for the disease pébrine in silkworms ( 1 ). Microsporidia are ubiquitous in the environment and infect almost all invertebrates and vertebrates, as well as some protists ( 2 ). Spores from microsporidia are commonly found in surface water ( 3 ). These organisms are eukaryotes that have a nucleus with a nuclear envelope, an intracytoplasmic membrane system, chromosome separation on mitotic spindles, vesicular Golgi, and a mitochondrial remnant organelle lacking a genome termed a mitosome ( 4 ). For insects, fish, laboratory rodents, and rabbits microsporidia are important pathogens, and they have been investigated as biological control agents for destructive species of insects ( 2 ). Several species of microsporidia have caused significant agricultural economic losses including Nosema apis and Nosema ceranae in honeybees ( 5 ), Loma salmonae in salmonid fish ( 6 ), and Thelohania species in shrimp ( 7 ). Franzen ( 8 ) published an excellent review of the history of research on these pathogens, and a recent textbook by Weiss and Becnel ( 2 ) provides a comprehensive examination of what is known about these organisms. In 1977 Sprague elevated the class or order Microsporidia to the phylum Microspora ( 9 ), and a decade later Sprague and Becnel ( 10 ) suggested that the term Microsporidia should instead be used for the phylum name. These organisms were previously considered “primitive” protozoa ( 11 ), but molecular phylogenetic analysis has resulted in the insight that these organisms are not primitive but instead are degenerate, and that Microsporidia are related to the Fungi, either as a basal branch of the Fungi or as a sister group ( 12 – 16 ).
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Microsporidian life cycles. The initial phase of infection involves spores being exposed to the proper environmental conditions that cause germination of the spores and polar tube extrusion. The polar tube pierces the plasma membrane (solid black line) of the host cell, and the sporoplasm travels through the polar tube into the host cell. The sporoplasm then divides during the proliferative phase, and the morphology of this division is used for determination of microsporidian genera. The sporoplasm on the left is uninucleate, and the cells that are produced from it represent the developmental patterns of several microsporidia with isolated nuclei. The sporoplasm on the right is diplokaryotic, and it similarly produces the various diplokaryotic developmental patterns. Cells containing either type of nucleation will produce one of three basic developmental forms. Some cycles have cells that divide immediately after karyokinesis by binary fission (e.g., Anncaliia). A second type forms elongated moniliform multinucleate cells that divide by multiple fission (e.g., some Nosema species). The third type forms rounded plasmodial multinucleate cells that divide by plasmotomy (e.g., Endoreticulatus species). Cells may repeat their division cycles one to several times in the proliferative phase. The intracellular stages in this phase are usually in direct contact with the host cell cytoplasm or closely abutted to the host endoplasmic reticulum; however, the proliferative cells of Encephalitozoon (and probably Tetramicra) are surrounded by a host-formed parasitophorous vacuole throughout their development, and the proliferative plasmodium of the genus Pleistophora is surrounded by a thick layer of parasite secretions that becomes the sporophorous vesicle in the sporogonic phase. The sporogonic phase is illustrated below the dashed line. Some of the microsporidian genera maintain direct contact with the host cell cytoplasm during sporogony, i.e., Nosema, Ichthyosporidium, Anncaliia, Enterocyotozoon, and probably Tetramicra. The remaining genera form a sporophorous vesicle as illustrated by the circles around developing sporogonial stages. It should be noted that in the Thelohania cycle and the Thelohania-like part of the Vairimorpha cycle, the diplokarya separate and continue their development as cells with isolated nuclei. Adapted with permission from reference 70 .
Microsporidian life cycles. The initial phase of infection involves spores being exposed to the proper environmental conditions that cause germination of the spores and polar tube extrusion. The polar tube pierces the plasma membrane (solid black line) of the host cell, and the sporoplasm travels through the polar tube into the host cell. The sporoplasm then divides during the proliferative phase, and the morphology of this division is used for determination of microsporidian genera. The sporoplasm on the left is uninucleate, and the cells that are produced from it represent the developmental patterns of several microsporidia with isolated nuclei. The sporoplasm on the right is diplokaryotic, and it similarly produces the various diplokaryotic developmental patterns. Cells containing either type of nucleation will produce one of three basic developmental forms. Some cycles have cells that divide immediately after karyokinesis by binary fission (e.g., Anncaliia). A second type forms elongated moniliform multinucleate cells that divide by multiple fission (e.g., some Nosema species). The third type forms rounded plasmodial multinucleate cells that divide by plasmotomy (e.g., Endoreticulatus species). Cells may repeat their division cycles one to several times in the proliferative phase. The intracellular stages in this phase are usually in direct contact with the host cell cytoplasm or closely abutted to the host endoplasmic reticulum; however, the proliferative cells of Encephalitozoon (and probably Tetramicra) are surrounded by a host-formed parasitophorous vacuole throughout their development, and the proliferative plasmodium of the genus Pleistophora is surrounded by a thick layer of parasite secretions that becomes the sporophorous vesicle in the sporogonic phase. The sporogonic phase is illustrated below the dashed line. Some of the microsporidian genera maintain direct contact with the host cell cytoplasm during sporogony, i.e., Nosema, Ichthyosporidium, Anncaliia, Enterocyotozoon, and probably Tetramicra. The remaining genera form a sporophorous vesicle as illustrated by the circles around developing sporogonial stages. It should be noted that in the Thelohania cycle and the Thelohania-like part of the Vairimorpha cycle, the diplokarya separate and continue their development as cells with isolated nuclei. Adapted with permission from reference 70 .
Diagram of a microsporidian spore. Spores range in size from 1 to 10 μm. The spore coat consists of an electron-dense exospore (Ex), an electron-lucent endospore (En), and a plasma membrane (Pm). It is thinner at the anterior end of the spore. The sporoplasm (Sp) contains a single nucleus (Nu), the posterior vacuole (PV), and ribosomes. The polar filament is attached to the anterior end of the spore by an anchoring disc (AD) and is divided into two regions: the manubroid, or straight portion (M), and the posterior region forming five coils (PT) around the sporoplasm. The manubroid polar filament is surrounded by the lamellar polaroplast (Pl) and vesicular polaroplast (VPl). The insert depicts a cross section of the polar tube coils (five coils in this spore), demonstrating the various concentric layers of different electron density and electron-dense core present in such cross sections. Reprinted with permission from reference 70 .
Diagram of a microsporidian spore. Spores range in size from 1 to 10 μm. The spore coat consists of an electron-dense exospore (Ex), an electron-lucent endospore (En), and a plasma membrane (Pm). It is thinner at the anterior end of the spore. The sporoplasm (Sp) contains a single nucleus (Nu), the posterior vacuole (PV), and ribosomes. The polar filament is attached to the anterior end of the spore by an anchoring disc (AD) and is divided into two regions: the manubroid, or straight portion (M), and the posterior region forming five coils (PT) around the sporoplasm. The manubroid polar filament is surrounded by the lamellar polaroplast (Pl) and vesicular polaroplast (VPl). The insert depicts a cross section of the polar tube coils (five coils in this spore), demonstrating the various concentric layers of different electron density and electron-dense core present in such cross sections. Reprinted with permission from reference 70 .
Scanning electron micrograph of microsporidia infection of a host cell shows the extruded polar tube of a spore of Encephalitozoon intestinalis piercing and infecting Vero E6 green monkey kidney cells in tissue culture. Reprinted with permission from reference 70 and with the kind permission of N. P. Kock, C. Schmetz, and J. Schottelius, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; published in Kock NP. 1998. Diagnosis of human pathogen microsporidia (dissertation).
Scanning electron micrograph of microsporidia infection of a host cell shows the extruded polar tube of a spore of Encephalitozoon intestinalis piercing and infecting Vero E6 green monkey kidney cells in tissue culture. Reprinted with permission from reference 70 and with the kind permission of N. P. Kock, C. Schmetz, and J. Schottelius, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; published in Kock NP. 1998. Diagnosis of human pathogen microsporidia (dissertation).
Species of microsporidia infecting humans
Species of microsporidia infecting humans