Opalinidae

Last updated

Opalinidae
Parasite140015-fig2 Protoopalina pingi (Opalinidae) Microscopy.tif
Protoopalina pingi [1]
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Stramenopiles
Phylum: Bigyra
Class: Opalinea
Order: Opalinida
Family: Opalinidae
Claus 1874
Genera

The opalines are a small group of peculiar heterokonts, currently assigned to the family Opalinidae, in the order Slopalinida. Their name is derived from the opalescent appearance of these microscopic organisms when illuminated with full sunlight. [2] Most opalines live in the large intestine and cloaca of anurans (frogs and toads), though they are sometimes found in fish, reptiles, molluscs and insects; whether they are parasitic is not certain. The unusual features of the opalines, first observed by Antonie van Leeuwenhoek in 1683, [3] has led to much debate regarding their phylogenetic position among the protists.

Contents

Taxonomy and phylogeny

The relationship between opalines and other protists has been a subject of great controversy since the late 19th century, and is not completely resolved at present. Initially, microscopists believed that the thousands of rhythmically beating hair-like structures which cover their surface were cilia, and they placed the opalines in Ciliophora. In the early 20th century other aspects of opaline biology clearly differentiated them from the ciliates [4] and they were placed in Sarcomastigophora, with the amoebae and flagellates. [5] In the 1980s, detailed ultrastructural studies of Opalina ranarum revealed that they share many features with the heterokonts of the family Proteromonadidae. A new order—Slopalinida Patterson 1985—was proposed to include the members of the families Proteromonadidae Grassé 1952 and Opalinidae Claus 1874. [6] In 2004, the first reliable opaline genetic sequence data supported the monophyletic nature of the order Slopalinida. [7] The authors of that study considered the opalines to be a family (Opalinidae) within the order Slopalinida.

There are currently about 200 recognized species of opalines in 5 genera: Opalina Purkinje and Valentin 1835, Protoopalina Metcalf 1918, Cepedea Metcalf 1920, Zelleriella Metcalf 1920, and Protozelleriella Delvinquier et al. 1991. Two additional genera, Hegneriella Earl 1971 and Bezzenbergeria Earl 1973, have not been considered as valid by subsequent authors (p. 249) [2] The 5 recognized genera differ in terms of the number of nuclei, the appearance and location of the falx (two short, sickle-shaped rows of flagella), and whether the long rows of flagella (called "kineties") cover the body evenly or if there is a "bald spot". Due to the differences in body shape among the different life cycle stages within a species, the use of overall body shape - whether flat or cylindrical - to differentiate the genera has been de-emphasized.

Life cycle

Protoopalina pingi from the recta of the frogs Sylvirana guentheri and Pelophylax nigromaculatus Parasite140015-fig3 Protoopalina pingi (Opalinidae) Drawing.tif
Protoopalina pingi from the recta of the frogs Sylvirana guentheri and Pelophylax nigromaculatus

Like many parasites, the life cycle of opalines is rather complex . The most comprehensive study published so far concluded that the life cycles of 10 Opalina species, 1 Zelleriella species and 1 Protoopalina species are all "remarkably similar" (p. 321). [8] A more recent study found that Cepedea couillardi fits the standard opaline life cycle model described below, while that of Opalina proteus is completed entirely in the tadpole stage of the host. [9] Very little is known about the life cycles of opalines in fish, reptile or arthropod hosts.

Asexual phase in adult anuran host. The basic opaline life cycle begins with the large, multinucleate trophonts in the adult anuran cloaca. Through much of the year, the trophonts grow and divide continually to yield more trophonts. Nuclear divisions maintain the appropriate number of nuclei during this phase. As the host's breeding season approaches, the trophonts enter a phase known as palintomy — a series of cell divisions with little or no overall growth or nuclear divisions. The resulting opalines, which become gradually smaller with fewer nuclei per individual, are called tomonts. At some point the small tomonts undergo encystment, and the cysts are released into the environment (i.e. the breeding pool of the anuran host) along with the feces.

Sexual and asexual phases in larval anuran host. Once cysts are eaten by foraging tadpoles, they excyst (hatch) to yield gamonts. The gamonts divide further, including a meiotic division, to yield haploid gametes. Each gamete has only one nucleus and may be either a microgamete or a macrogamete. Conjugation occurs between one microgamete and one macrogamete, to yield a diploid zygocyst with one nucleus. The zygocyst has two possible fates. It may be shed along with the feces of the tadpole host; and if eaten by another tadpole, it will excyst (hatch) to yield more gamonts in the new host. Alternatively, the zygocyst may excyst in its original host and grow into a multinucleate protrophont. In this case, the protrophont grows into a trophont and the whole cycle starts over again. The cycle from protrophont to cyst may occur in either the tadpole or adult hosts. Some evidence suggests that the life cycle transitions of opalines may be governed by the hormonal cycles of the host. [10]

Hosts and commensal lifestyle

Lacking a mouth, opalines feed by taking in nutrients from their surroundings by pinocytosis. While the opalines are often referred to as "parasites", two lines of evidence suggest that they are actually commensals which do no harm to their anuran hosts.

  1. They are found almost exclusively in the large intestine and cloaca. Since the anuran absorbs the nutrients from its food in the small intestine, the opalines are probably not depriving their hosts of nutrients. It is believed that the opalines are simply living off the "left-over" nutrients in the feces, possibly supplemented by the biochemical contributions of the rich bacterial flora which also reside there.
  2. Anuran hosts containing many thousands of opalines appear to be completely healthy, with no obvious irritation or other pathological signs on their intestinal or cloacal walls.

Only about a dozen reports of opalines in fishes have been published, and even fewer on opalines from reptile or salamander hosts. Their scarcity outside of anuran hosts had led many to speculate that the others are just incidental infestations—maybe the infested snake had just eaten an infested frog, for example. However, opalines have been found in saltwater fish which have no access to anurans. Also, the populations of opalines in fish hosts are often very high, suggesting that they are probably reproducing in the fish host. [11]

The pathogenicity (if any) of opalines in fish hosts is not yet known. One study found no irritation or other pathological signs on the rectal epithelium of Symphysodon aequifasciata infested with Protoopalina symphysodonis, but stated that "most infected animals died". [12]

In vitro culture of opalines

Successful culturing of opalines in artificial media for periods of 1 month or more has been reported. [13] This technique will aid tremendously in future studies of all aspects of opaline biology.

Related Research Articles

<span class="mw-page-title-main">Apicomplexa</span> Phylum of parasitic alveolates

The Apicomplexa are organisms of a large phylum of mainly parasitic alveolates. Most possess a unique form of organelle structure that comprises a type of non-photosynthetic plastid called an apicoplast—with an apical complex membrane. The organelle's apical shape is an adaptation that the apicomplexan applies in penetrating a host cell.

<i>Entamoeba</i> Genus of internal parasites

Entamoeba is a genus of Amoebozoa found as internal parasites or commensals of animals. In 1875, Fedor Lösch described the first proven case of amoebic dysentery in St. Petersburg, Russia. He referred to the amoeba he observed microscopically as Amoeba coli; however, it is not clear whether he was using this as a descriptive term or intended it as a formal taxonomic name. The genus Entamoeba was defined by Casagrandi and Barbagallo for the species Entamoeba coli, which is known to be a commensal organism. Lösch's organism was renamed Entamoeba histolytica by Fritz Schaudinn in 1903; he later died, in 1906, from a self-inflicted infection when studying this amoeba. For a time during the first half of the 20th century the entire genus Entamoeba was transferred to Endamoeba, a genus of amoebas infecting invertebrates about which little is known. This move was reversed by the International Commission on Zoological Nomenclature in the late 1950s, and Entamoeba has stayed 'stable' ever since.

<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.

<i>Entamoeba coli</i> Species of parasitic amoeba

Entamoeba coli is a non-pathogenic species of Entamoeba that frequently exists as a commensal parasite in the human gastrointestinal tract. E. coli is important in medicine because it can be confused during microscopic examination of stained stool specimens with the pathogenic Entamoeba histolytica. This amoeba does not move much by the use of its pseudopod, and creates a "sur place (non-progressive) movement" inside the large intestine. Usually, the amoeba is immobile, and keeps its round shape. This amoeba, in its trophozoite stage, is only visible in fresh, unfixed stool specimens. Sometimes the Entamoeba coli have parasites as well. One is the fungus Sphaerita spp. This fungus lives in the cytoplasm of the E. coli. While this differentiation is typically done by visual examination of the parasitic cysts via light microscopy, new methods using molecular biology techniques have been developed. The scientific name of the amoeba, E. coli, is often mistaken for the bacterium, Escherichia coli. Unlike the bacterium, the amoeba is mostly harmless, and does not cause as many intestinal problems as some strains of the E. coli bacterium. To make the naming of these organisms less confusing, "alternate contractions" are used to name the species for the purpose making the naming easier; for example, using Esch. coli and Ent. coli for the bacterium and amoeba, instead of using E. coli for both.

<i>Echinococcus multilocularis</i> Species of flatworm

Echinococcus multilocularis, the fox tapeworm, is a small cyclophyllid tapeworm found extensively in the northern hemisphere. E. multilocularis, along with other members of the Echinococcus genus, produce diseases known as echinococcosis. Unlike E. granulosus,E. multilocularis produces many small cysts that spread throughout the internal organs of the infected animal. The resultant disease is called Alveolar echinococcosis, and is caused by ingesting the eggs of E. multilocularis.

<span class="mw-page-title-main">Velvet (fish disease)</span> Parasitic disease of fish

Velvet disease is a fish disease caused by dinoflagellate parasites of the genera Amyloodinium in marine fish, and Oodinium in freshwater fish. The disease gives infected organisms a dusty, brownish-gold color. The disease occurs most commonly in tropical fish, and to a lesser extent, marine aquaria. Periodic use of preventive treatments like aquarium salt can further deter parasites. Regular monitoring, attentive care, and preventive measures collectively contribute to keeping fish healthy and velvet-free.

<i>Retortamonas</i> Unicellular organism

Retortamonas is a genus of flagellated excavates. It is one of only two genera belonging to the family Retortamonadidae along with the genus Chilomastix. The genus parasitizes a large range of hosts including humans. Species within this genus are considered harmless commensals which reside in the intestine of their host. The wide host diversity is a useful factor given that species are distinguished based on their host rather than morphology. This is because all species share similar morphology, which would present challenges when trying to make classifications based on structural anatomy. Although Retortamonas currently includes over 25 known species, it is possible that some defined species are synonymous, given that such overlapping species have been discovered in the past. Further efforts into learning about this genus must be done such as cross-transmission testing as well as biochemical and genetic studies. One of the most well-known species within this genus is Retortamonas intestinalis, a human parasite that lives in the large intestine of humans.

Capillaria philippinensis is a parasitic nematode which causes intestinal capillariasis. This sometimes fatal disease was first discovered in Northern Luzon, Philippines, in 1964. Cases have also been reported from China, Egypt, Indonesia, Iran, Japan, Korea, Lao PDR, Taiwan and Thailand. Cases diagnosed in Italy and Spain were believed to be acquired abroad, with one case possibly contracted in Colombia. The natural life cycle of C. philippinensis is believed to involve fish as intermediate hosts, and fish-eating birds as definitive hosts. Humans acquire C. philippinensis by eating small species of infested fish whole and raw.

Ribeiroia ondatrae, or the frog-mutating flatworm is a parasite in the genus Ribeiroia which is believed to be responsible for many of the recent increases in amphibian limb malformations, particularly missing, malformed, and additional hind legs.

<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.

<i>Nanophyetus</i> Genus of flukes

Nanophyetus salmincola is a food-borne intestinal trematode parasite prevalent on the Pacific Northwest coast. The species may be the most common trematode endemic to the United States.

<span class="mw-page-title-main">Bigyra</span> Phylum of single-celled organisms

Bigyra is a phylum of microscopic eukaryotes that are found at the base of the Stramenopiles clade. It includes three well-known heterotrophic groups Bicosoecida, Opalinata and Labyrinthulomycetes, as well as several small clades initially discovered through environmental DNA samples: Nanomonadea, Placididea, Opalomonadea and Eogyrea. The classification of Bigyra has changed several times since its origin, and its monophyly remains unresolved.

<span class="mw-page-title-main">Adeleorina</span> Suborder of microscopic, spore-forming, single-celled parasites in the aplcomplex phylum

Adeleorina is a suborder of parasites in the phylum Apicomplexa.

<i>Proteromonas</i> Genus of single-celled organisms

Proteromonas is a genus of single-celled biflagellated microbial eukaryotes belonging to the Superphylum Stramenopiles which are characterized by the presence of tripartite, hair-like structures on the anteriorly-directed larger of the two flagella. Proteromonas on the other hand are notable by having tripartite hairs called somatonemes not on the flagella but on the posterior of the cell. Proteromonas are closely related to Karotomorpha and Blastocystis, which belong to the Opalines group.

Dendronucleata is a genus of small parasitic spiny-headed worms. It is the only genus in the family Dendronucleatidae. This genus contains three species that are distributed globally, being collected in North America and Asia. The distinguishing features of this genus among Archiacanthocephalans is the presence of randomly distributed dendritically branched giant hypodermic nuclei. Dendronucleata parasitize freshwater fish and a salamander by attaching themselves in the intestines using their hook covered proboscis and adhesives secreted from cement glands.

Entamoeba invadens is an amoebozoa parasite of reptiles, within the genus Entamoeba. It is closely related to the human parasite Entamoeba histolytica, causing similar invasive disease in reptiles, in addition to a similar morphology and lifecycle.

Amyloodinium ocellatum is a cosmopolitan ectoparasite dinoflagellate of numerous aquatic organisms living in brackish and seawater environments. The dinoflagellate is endemic in temperate and tropical areas, and is capable of successfully adapting to a variety of different environments and to a great number of hosts, having been identified in four phyla of aquatic organisms: Chordata, Arthropoda, Mollusca and Platyhelminthes. Moreover, it is the only dinoflagellate capable of infecting teleosts and elasmobranchs.

<i>Chilomastix</i>

Chilomastix is a genus of pyriform excavates within the family Retortamonadidae All species within this genus are flagellated, structured with three flagella pointing anteriorly and a fourth contained within the feeding groove. Chilomastix also lacks Golgi apparatus and mitochondria but does possess a single nucleus. The genus parasitizes a wide range of vertebrate hosts, but is known to be typically non-pathogenic, and is therefore classified as harmless. The life cycle of Chilomastix lacks an intermediate host or vector. Chilomastix has a resistant cyst stage responsible for transmission and a trophozoite stage, which is recognized as the feeding stage. Chilomastix mesnili is one of the more studied species in this genus due to the fact it is a human parasite. Therefore, much of the information on this genus is based on what is known about this one species.

<i>Echinococcus vogeli</i> Species of flatworm

Echinococcus vogeli is a small cyclophyllid tapeworm found in Central and South America. E. vogeli, as well as other members of the genus Echinococcus, produce a disease called echinococcosis. Echinococcosis, also known has hydatidosis, is a result of ingesting the eggs of the genus Echinococcus. E. vogeli is similar to E. multilocularis in that both species produces many small cysts that spread throughout the internal organs of the infected animal. The ingestion of E. vogeli eggs, and the spreading of the cysts through infected host, will results in Polycystic Echinococcosis.

<span class="mw-page-title-main">Cat worm infections</span> Worm infections in cats

Cat worm infections, the infection of cats (Felidae) with parasitic worms, occur frequently. Most worm species occur worldwide in both domestic and other cats, but there are regional, species and lifestyle differences in the frequency of infestation. According to the classification of the corresponding parasites in the zoological system, infections can be divided into those caused by nematode and flatworms - in the case of the latter, mainly cestoda and trematoda - while other strains are of no veterinary significance. While threadworms usually do not require an intermediate host for their reproduction, the development cycle of flatworms always proceeds via alternate hosts.

References

  1. 1 2 Li, Weidong; Wang, Chong; Huang, Feng; Li, Ming; Nilsen, Frank; Liu, Huiyu; Xu, Jianlong (2014). "Redescription of Protoopalina pingi Nie, 1935 inhabiting the recta of Hylarana guentheri and Pelophylax nigromaculatus in China". Parasite. 21: 46. doi:10.1051/parasite/2014021. PMC   4160848 . PMID   25208482. Open Access logo PLoS transparent.svg
  2. 1 2 Delvinquier, .L.J.; Patterson, D.J. (1993). "The opalines". In Kreier, Julius P.; Baker, John R. (eds.). Parasitic Protozoa. Vol. 3 (2nd ed.). Academic Press. pp. 247–325. ISBN   978-0-12-426013-9.
  3. Dobell, C. (1932). Antony van Leeuwenhoek and his "little animals". London: Bale, Sons and Danielson.
  4. Corliss, J.O. (1955). "The opalinid infusorians: Flagellates or ciliates?". Journal of Protozoology. 2 (3): 107–114. doi:10.1111/j.1550-7408.1955.tb02410.x.
  5. Corliss, J.O.; Balamuth, W. (1963). "Consideration of the opalinids as a new superclass in the subphylum Sarcomastigophora". Journal of Protozoology. 10 (Suppl): 26.
  6. Patterson, D.J. (1985). "The fine structure of Opalina ranarum (family Opalinidae): Opalinid phylogeny and classification". Protistologica. 21 (4): 413–428.
  7. Kostka M, Hampl V, Cepicka I, Flegr J (2004). "Phylogenetic position of Protoopalina intestinalis based on SSU rRNA gene sequence". Mol. Phylogenet. Evol. 33 (1): 220–4. doi:10.1016/j.ympev.2004.05.009. PMID   15324850.
  8. Wessenberg, H. (1961). "Studies on the life cycle and morphogenesis of Opalina". University of California Studies in Zoology. 61 (6): 315–370.
  9. Affa'a, F.-M.; Mignot, J.-P.; Amiet, J.-L. (1996). "Morphological and cytological observations on two opalinid endocommensals of Acanthixalus spinosus (Amphibia, Anura)". Canadian Journal of Zoology. 74 (8): 1573–84. doi:10.1139/z96-171.
  10. El Mofty MM, Sadek IA (1975). "The effect of fresh toad bile on the induction of encystation in Opalina sudafricana parasitic in Bufo regularis". Int. J. Parasitol. 5 (2): 219–24. doi:10.1016/0020-7519(75)90032-6. PMID   803935.
  11. Sandon, H. (1980). "Notes on African opalinids (Protozoa, Opalinata). 1. Zelleriella spp". Systematic Parasitology. 1 (3–4): 171–188. doi:10.1007/BF00009844.
  12. Foissner, W.; Schubert, G.; Wilbert, N. (1979). "Morphologie, Infraciliatur und Silberliniensystem von Protoopalina symphysodonis nov. spec. (Protozoa: Opalinata), einer Opalinidae aus dem Intestinum von Symphysodon aequifasciata Pellegrin (Percoidei: Cichlidae.)". Zoologischer Anzeiger. 202 (1–2): 71–85.
  13. Hanamura, K.; Endoh, H. (2001). "Binary fission and encystation of Opalina sp. in axenic medium" (PDF). Zoological Science. 18 (3): 381–7. doi:10.2108/zsj.18.381. Archived from the original (PDF) on 2017-10-25. Retrieved 2008-11-14. (and references cited therein)