Xenoma

Last updated
Xenoma on the flatfish Limanda limanda Glugea stephani.jpg
Xenoma on the flatfish Limanda limanda

A xenoma (also known as a 'xenoparasitic complex') is a growth caused by various protists and fungi, most notably microsporidia. It can occur on numerous organisms; however is predominantly found on fish. [1]

Contents

In most cases the host cell and nuclei suffers from hypertrophy resulting in a change in organisation of the cell and its structure and can result in polyploid nuclei. This outcome is due to the microsporidian parasite proliferating inside the host cell. This results in a 'symbiotic co-existence' between the parasite and the host cell. [1] This forms the xenoparasitic complex. They tend to contain numerous cellular components as well as microsporidia at different developmental stages and spores. [2]

Not all microsporidia infections result in the formation of xenomas; only a few microsporidia actually cause xenoma formation. [2]

History

Xenoparasitic complex was the term initially devised in the early twentieth century to describe specific type 'tumours' found on various organisms, specific as the infections were caused by multiple subclasses of microsporidia. A paper published in 1922 by Weissenberg came up with the term 'xenon' for the xenoparasitic complexes he observed on sticklebacks caused by Glugea anomala , before eventually changing it to xenoma (xenon was already the name of a newly discovered chemical element). [1] [3]

Hypertrophy of cells caused by protists and fungi has been observed since the late nineteenth century. Scientists observed them in several organisms, of which the infection would have varied host cell specificity, ultimately leading to different cellular consequences. [1] For example, the dinoflagellate protist Sphaeripara catenata induces hypertrophy, polyploid nuclei formation whilst forming a thick-walled hyposome where rhizoids extend into the cytoplasm for nutrient absorption in the appendicularian Fritillaria pellucida. [1] [4] This can be contrasted to the Microsporidium cotti infection of the testes of Taurulus bubalis where a dense microvillus layer is present for improved nutrient absorption. [1] [5]

Pathogenesis

Xenomas are provoked in various types of organisms, depending on the species of the parasite. Microsporidia are known to produce xenomas in oligochaetes, insects, crustaceans and fish. [1] In addition to organism specificity, different species of parasite will have distinct host cell specificity, even if targeting the same organism. For example, Microsporidium chaetogastris infects solely connective and muscle tissue cells of the annelid Chaetogaster diaphanus, [6] whereas other species of microsporidia will target other tissue types. Another example is microsporidial gill disease in different species of fish caused by Loma salmonae . It was found that certain species had a higher prevalence of xenoma formation following infection with the same parasite i.e. xenomas per gill filament in chinook salmon was 8 to 33 times greater than in rainbow trout, showing differences in host cell susceptibility. [7]

Once a host cell is infected with the microsporidian (or protist) parasite, a complete restructuring of the host cell ensues. This occurs as the parasite seeks to take control of the metabolism of the cell, in order to survive and exploit the host cell's resources and reproduction. It provides the parasite with optimal growth conditions and protection from the host's immune response. The parasite proliferates within the host cell where its mass replaces most of the host cell's cytoplasm, with the rest being taken up by microvillus structures and rhizoids. Other structures may be present inside the infected host cell including vesicles, fat globules and bundles of fibril. The nucleus may be in varying locations including the centre of the cell and may also vary in structure i.e. lobed, branched or divided into multiple fragments, but it will always be hypertrophic. [1] The host also commonly envelops the proliferating parasite and the host cell itself in layers of membranes and cells. [2]

In microsporidian xenomas the whole life cycle is restricted to the xenoma; this however differs between different protists. [1] The life cycle predominantly follows a simple life cycle consisting of merogony followed by sporogony. Occasionally the endoplasmic reticulum associates with meronts, which are formed during merogony, and is lost once sporogony ensues. [8] The time it takes for a xenoma to develop varies entirely on the host organism and cell as well as the infecting parasite. It can vary, however it usually starts to form after a few weeks following infection, depending on the life cycle of the parasite. The size of xenomas also varies with the type of parasite and host organism, and can range from a few micrometres to several millimetres. [1]

While it is generally accepted that the xenoma prevents spread of the parasite throughout the host organism, it is not entirely accurate. As the species that cause xenomas are spore-forming, it is possible that their spores may release their sporoplasms which penetrate the xenoma wall, infiltrating and infecting surrounding cells. In microsporidia this is mediated by a unique and highly specialised protein: the polar tube. This specialised protein is found inside the spore and is in contact with the sporoplasm. Specific environmental stimulation causes the spore to discharge the polar tube which penetrates the xenoma membrane and provides an exit route for the sporoplasm. This is thought to be a form of autoinfection. [1] Rupture of the xenoma may also result in dispersal of the infectious spores. [1] This can lead to the formation of other and more persistent forms of xenomas. [2]

Transmission of such pathogens occurs predominantly via oral administration when in contact or in the vicinity of diseased organisms via the release of infectious spores. However, there are reports of obtaining infection in some organisms through the skin. [9] Experimentally inducing infection and xenoma formation can be performed intramuscularly, intravascularly and intraperitoneally. [1] It is widely thought that the first site of entry for many of these parasites is in the gastrointestinal tract where enzymes such as pepsin or even an alkaline pH shift (caused by the mucous layer prominent in this area) induces polar tube discharge. [1] [10] Following this their migration from their initial release to their final destination in the host cell varies considerably, depending on the pathogen, the host organism and the host cell location. It was discovered through in situ hybridization that the microsporidia Loma salmonae enters the mucosal epithelium in the intestine and migrates to the lamina propria before arriving at the gills, where it eventually resides, via infecting blood cells. [11] Other transport vehicles are thought to include T cells, lymphocytes, and other migratory cells including monocytes where they succumb to infection by means of either phagocytosis of the parasite in the lamina propria or by infiltration by sporoplasms using their polar tube. It is also very possible that these transport cells might themselves develop into a xenoma. [1]

Xenomas in fish

Microsporidia is a common cause of disease in fish and so xenomas tend to be seen more frequently in fish than in other organisms. A paper published in 2002 listed 15 genera and 157 microsporidian species that cause disease in fish, [2] [12] however only ten of these genera induce xenoma formation. [8] Microsporidia genera that cause xenomas can therefore be quite diverse and so are characterised more comprehensively into several groups depending on their morphology: [1]

Recently fish-infecting microsporidia have been grouped into five classes depending on their molecular traits, a higher level of classification using SSU (small subunit) rDNA analysis. However molecular data is still lacking for several genera of microsporidia. [13]

Xenomas found in other organisms

Whilst xenomas are more highly characteristic of fish, they can be quite extensive in other organisms including crustaceans, insects, oligochaetes and other vertebrates. Microsporidian xenomas that develop in fish can also occur in crustaceans. [1] Roughly 43 microsporidian genera have been found to infect crustaceans, with at least 23 microsporidian species found in shrimp, most of them infecting muscular tissue. [14] Other species also infect the digestive tract, reproductive organs and their hepatopancreas. [14] Xenoma-like formations have also been found in species of shrew caused by Soricimyxum fegati, a type of myxosporea, showing they can also occur in mammals. [15]

Treatment

The host can eventually destroy the xenoma. Proliferative inflammation occurs in mature xenomas and transforms them into granulomas. Granuloma involution then ensues where phagocytosis kills the spores. [1]

Studies have shown it is possible to vaccinate against xenomas. One study showed that developing a vaccine using a 103 to 105 dose of killed spores from a low-virulence strain of Loma salmonae resulted in rainbow trout producing 85% less xenomas in their gills after experimental infection (compared to the control). This ultimately offers much improved protection to microsporidial gill disease which is common amongst rainbow trout. [16] Therapeutic drugs have proved ineffective at treating this disease and harvesting whole-spores is a relatively easy technique. [16]

See also

Related Research Articles

<span class="mw-page-title-main">Myxozoa</span> Group of marine parasites

Myxozoa is a subphylum of aquatic cnidarian animals – all obligate parasites. It contains the smallest animals ever known to have lived. Over 2,180 species have been described and some estimates have suggested at least 30,000 undiscovered species. Many have a two-host lifecycle, involving a fish and an annelid worm or a bryozoan. The average size of a myxosporean spore usually ranges from 10 μm to 20 μm, whereas that of a malacosporean spore can be up to 2 mm. Myxozoans can live in both freshwater and marine habitats.

<i>Ichthyophthirius multifiliis</i> Parasitic species of protozoan

Ichthyophthirius multifiliis, often termed "Ich", is a parasitic ciliate described by the French parasitologist Fouquet in 1876. Only one species is found in the genus which also gave name to the family. The name literally translates as "the fish louse with many children". The parasite can infect most freshwater fish species and, in contrast to many other parasites, shows low host specificity. It penetrates gill epithelia, skin and fins of the fish host and resides as a feeding stage inside the epidermis. It is visible as a white spot on the surface of the fish but, due to its internal microhabitat, it is a true endoparasite and not an ectoparasite.

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).

<span class="mw-page-title-main">Microsporidia</span> Phylum of fungi

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. They were once considered protozoans or protists, but are now known to be fungi, or a sister group to fungi. These fungal microbes are obligate eukaryotic parasites that use a unique mechanism to infect host cells. 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 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 species are parasites of vertebrates —several species, most of which are opportunistic, can infect humans, in whom they can cause microsporidiosis.

<i>Myxobolus cerebralis</i> Species of parasite

Myxobolus cerebralis is a myxosporean parasite of salmonids that causes whirling disease in farmed salmon and trout and also in wild fish populations. It was first described in rainbow trout in Germany in 1893, but its range has spread and it has appeared in most of Europe, the United States, South Africa, Canada and other countries from shipments of cultured and wild fish. In the 1980s, M. cerebralis was found to require a tubificid oligochaete to complete its life cycle. The parasite infects its hosts with its cells after piercing them with polar filaments ejected from nematocyst-like capsules. This infects the cartilage and possibly the nervous tissue of salmonids, causing a potentially lethal infection in which the host develops a black tail, spinal deformities, and possibly more deformities in the anterior part of the fish.

Tetracapsuloides bryosalmonae is a myxozoan parasite of salmonid fish. It is the only species currently recognized in the monotypic genus Tetracapsuloides. It is the cause of proliferative kidney disease (PKD), one of the most serious parasitic diseases of salmonid populations in Europe and North America that can result in losses of up to 90% in infected populations.

The Vannellidae are a family of Amoebozoa, which are found in soil, fresh- and salt water. The most common genus is Vannella.

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.

Enterocytozoon bieneusi is a species of the order Chytridiopsida which infects the intestinal epithelial cells. It is an obligate intracellular parasite.

Glugea is a genus of microsporidian parasites, predominantly infecting fish. Infections of Glugea cause xenoma formation.

Loma is a genus of microsporidian parasites, infecting fish. The taxonomic position of Loma in the family Glugeidae has been questioned by DNA sequencing results.

<span class="mw-page-title-main">Protozoan infection</span> Parasitic disease caused by a protozoan

Protozoan infections are parasitic diseases caused by organisms formerly classified in the kingdom Protozoa. These organisms are now classified in the supergroups Excavata, Amoebozoa, Harosa, and Archaeplastida. They are usually contracted by either an insect vector or by contact with an infected substance or surface.

Encephalitozoon intestinalis is a parasite. It can cause microsporidiosis.

<span class="mw-page-title-main">Fish diseases and parasites</span> Disease that affects fish

Like humans and other animals, fish suffer from diseases and parasites. Fish defences against disease are specific and non-specific. Non-specific defences include skin and scales, as well as the mucus layer secreted by the epidermis that traps microorganisms and inhibits their growth. If pathogens breach these defences, fish can develop inflammatory responses that increase the flow of blood to infected areas and deliver white blood cells that attempt to destroy the pathogens.

<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.

Loma salmonae is a species of microsporidian parasite, infecting Pacific salmon. L. salmonae is the causative agent of microsporidial gill disease of salmon. It is an intracellular parasite which induces respiratory distress, secondary infection, and increased mortality rates.

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>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.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 Lom J, Dyková I (2005). "Microsporidian xenomas in fish seen in wider perspective". Folia Parasitologica. 52 (1–2): 69–81. doi: 10.14411/fp.2005.010 . PMID   16004366.
  2. 1 2 3 4 5 Matos E, Corral L, Azevedo C (2003). "Ultrastructural details of the xenoma of Loma myrophis (phylum Microsporidia) and extrusion of the polar tube during autoinfection". Diseases of Aquatic Organisms. 54 (3): 203–207. doi: 10.3354/dao054203 . PMID   12803384.
  3. Weissenberg R. "Mikrosporidien und Chlamydozoen als Zellparasiten von Fischen". Verh. Dtsch. Zool. Ges. 27: 41–43.
  4. Chatton E. "Un complexe xéno-parasitaire morphologique et physiologique Neresheimeria paradoxa chez Fritillaria pellucida". C. R. Acad. Sci. Paris. 171: 55–57.
  5. Chatton E, Courrier R. "Formation d'un complexe xénoparasitaire géant avec bordure en brosse, sous l'influence d'une Microsporidie, dans le testicule de Cottus bubalis". C. R. Soc. Biol. (Paris). 89: 579–583.
  6. Schröder O. "Thelohania chaetogastris, eine neue in Chaetogaster diaphanus Gruith schmarotzende Microsporidienart". Arch. Protistenkd. 14: 119–133.
  7. Ramsay JM, Speare DJ, Dawe SC, Kent ML (2002). "Xenoma formation during microsporidial gill disease of salmonids caused by Loma salmonae is affected by host species (Oncorhynchus tshawytscha, O. kisutch, O. mykiss) but not by salinity". Diseases of Aquatic Organisms. 48 (2): 125–131. doi: 10.3354/dao048125 . PMID   12005234.
  8. 1 2 Mansour L, Prensier G, Jemaa SB, Hassine OK, Méténier G, Vivarès CP, Cornillot E (2005). "Description of a xenoma-inducing microsporidian, Microgemma tincae n. sp., parasite of the teleost fish Symphodus tinca from Tunisian coasts". Diseases of Aquatic Organisms. 65 (3): 217–226. doi: 10.3354/dao065217 . PMID   16119890.
  9. Lee SJ, Yokoyama H, Ogawa K (2004). "Modes of transmission of Glugea plecoglossi (Microspora) via the skin and digestive tract in an experimental infection model using rainbow trout, Oncorhyncus mykiss (Walbaum)". J. Fish Dis. 27 (8): 435–444. Bibcode:2004JFDis..27..435L. doi:10.1111/j.1365-2761.2004.00556.x. PMID   15291785.
  10. Lee SJ, Yokoyama H, Ogawa K (2003). "Rapid in situ hybridisation technique for the detection of fish microsporidian parasites". Fish Pathol. 38 (3): 117–119. doi: 10.3147/jsfp.38.117 .
  11. Sánchez JG, Speare DJ, Markham RJ, Wright GM, Kibenge FS (2016). "Localization of the initial developmental stages of Loma salmonae in rainbow trout (Oncorhynchus mykiss)". Vet. Pathol. 38 (5): 540–546. doi: 10.1354/vp.38-5-540 . PMID   11572561.
  12. Lom J (2002). "A catalogue of described genera and species of microsporidians parasitic in fish". Syst Parasitol. 53 (2): 81–99. doi:10.1023/a:1020422209539. PMID   12386417.
  13. Lom J, Nilsen F (2003). "Fish microsporidia: fine structural diversity and phylogeny". International Journal for Parasitology. 33 (2): 107–127. doi:10.1016/s0020-7519(02)00252-7.
  14. 1 2 Wang TC, Nai YS, Wang CY, Solter LF, Hsu HC, Wang CH, Lo CF (2013). "A new microsporidium, Triwangia caridinae gen. nov., sp. Nov. parasitizing fresh water shrimp, Caridina formosae (Decapoda: Atyidae) in Taiwan". Journal of Invertebrate Pathology. 112 (3): 281–293. Bibcode:2013JInvP.112..281W. doi:10.1016/j.jip.2012.12.014. PMID   23318886.
  15. Dyková I, Tyml T, Kostka M (2011). "Xenoma-like formations induced by Soricimyxum fegati (Myxosporea) in three species of shrews (Soricomorpha: Soricidae), including records of new hosts". Folia Parasitologica. 58 (4): 249–256. doi: 10.14411/fp.2011.024 . PMID   22263306.
  16. 1 2 Speare DJ, Markham RJ, Guselle NJ (2007). "Development of an Effective Whole-Spore Vaccine To Protect against Microsporidial Gill Disease in Rainbow Trout (Oncorhyncus mykiss) by Using a Low-Virulence Strain of Loma salmonae". Clinical and Vaccine Immunology. 14 (12): 1652–1654. doi:10.1128/CVI.00365-07. PMC   2168380 . PMID   17942613.