Gregarinasina

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Gregarinasina
Septate gregarine.jpg
A live specimen of a septate (or cephaline) gregarine showing the distinctive "head"-like section of the trophozoite containing the epimerite at its anterior end. Septate gregarines are intestinal parasites of arthropods.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Apicomplexa
Class: Conoidasida
Subclass: Gregarinasina
Orders

Archigregarinorida
Eugregarinorida
Neogregarinorida

Contents

Synonyms
  • Gregarinia

The gregarines are a group of Apicomplexan alveolates, classified as the Gregarinasina [1] or Gregarinia. The large (roughly half a millimeter) parasites inhabit the intestines of many invertebrates. They are not found in any vertebrates. Gregarines are closely related to both Toxoplasma and Plasmodium , which cause toxoplasmosis and malaria, respectively. Both protists use protein complexes similar to those that are formed by the gregarines for gliding motility and for invading target cells. [2] [3] This makes the gregarines excellent models for studying gliding motility, with the goal of developing treatment options for both toxoplasmosis and malaria. Thousands of different species of gregarine are expected to be found in insects, and 99% of these gregarine species still need to be described. Each insect species can be the host of multiple gregarine species. [4] [5] One of the most-studied gregarines is Gregarina garnhami . In general, gregarines are regarded as a very successful group of parasites, as their hosts are distributed over the entire planet. [6]

Life cycle

Gregarines occur in both aquatic and terrestrial environments. Although they are usually transmitted by the orofaecal route, some are transmitted with the host's gametes during copulation, e.g., Monocystis .

In all species, four or more sporozoites (depending on the species), equipped with an apical complex, escape from the oocysts in a process called excystation. They find their way to the appropriate body cavity, and penetrate host cells in their immediate environment. The sporozoites begin to feed within the host cell and develop into larger trophozoites. In some species, the sporozoites and trophozoites are capable of asexual replication – a process called schizogony or merogony.

In all species, two mature trophozoites eventually pair up in a process known as syzygy and develop into gamonts. During syzygy, gamont orientation differs between species (side-to-side, head-to-tail). A gametocyst wall forms around each gamont pair, which then begins to divide into hundreds of gametes. Zygotes are produced by the fusion of two gametes, and these, in turn, become surrounded by an oocyst wall. Within the oocyst, meiosis occurs, yielding the sporozoites. Hundreds of oocysts accumulate within each gametocyst; these are released via a host's faeces or via host death and decay.

Lankesteria cystodytae is an intestinal parasite of ascidians. These aseptate gregarines lack epimerites and instead possess attachment organelles known as mucrons Lankesteria lm.jpg
Lankesteria cystodytae is an intestinal parasite of ascidians. These aseptate gregarines lack epimerites and instead possess attachment organelles known as mucrons

Gregarines have thus far been reported to infect over 3000 invertebrate species. [7]

Taxonomy

The gregarines were recognised as a taxon by Grasse in 1953. [8] The three orders into which they are currently divided were created by Levine et al. in 1980.

Currently, about 250 genera and 1650 species are known in this taxon. They are divided into three orders based on habitat, host range, and trophozoite morphology. [9]

Most species have monoxenous lifecycles involving a single invertebrate host. In the lifecycle, the extracellular feeding stage is known as the trophozoite.

Main divisions

Archigregarines are found only in marine habitats. They possess intestinal trophozoites similar in morphology to the infective sporozoites. Phylogenetic analysis suggests this group is paraphyletic and will need division. Generally, four zoites are in each spore in this group.

Eugregarines are found in marine, freshwater, and terrestrial habitats. These species possess large trophozoites that are significantly different in morphology and behavior from the sporozoites. This taxon contains most of the known gregarine species. The intestinal eugregarines are separated into septate – suborder Septatorina – and aseptate – suborder Aseptatorina – depending on whether the trophozoite is superficially divided by a transverse septum. The aseptate species are mostly marine gregarines.

Urosporidians are aseptate eugregarines that infect the coelomic spaces of marine hosts. Unusually, they tend to lack attachment structures and form gamont pairs that pulsate freely within the coelomic fluid.

Monocystids are aseptate eugregarines that infect the reproductive vesicles of terrestrial annelids. These latter species tend to branch closely with neogregarines and may need to be reclassified. Generally, eight zoites are in each spore in this group.

Neogregarines are found only in terrestrial hosts. These species have reduced trophozoites and tend to infect tissues other than the intestine. Usually, eight zoites are in each spore in this group.

The eugregarines and neogregarines differ in a number of respects. The neogregarines are in general more pathogenic to their hosts. The eugregarines multiply by sporogony and gametogony, while the neogregarines have an additional schizogenic stage – merogony – within their hosts. Merogony may be intracellular or extracellular depending on the species.

DNA studies suggest the archigregarines are ancestral to the others. [10]

Proposed revisions

Cavalier-Smith has proposed a significant revision of this taxon assuming the polyphyly of eugregarines. [11] He has separated gregarines into three classes. The first of them – Gregarinomorphea – comprises Orthogregarinia, Cryptosporidiidae and, additionally, Rhytidocystidae previously considered as divergent coccidians [9] or Apicomplexa incertae sedis. [12] The Orthogregarinia with two new orders Arthrogregarida and Vermigregarida was created for the gregarines most closely related to Cryptosporidium . The second class – Paragregarea – was created for the archigregarines, Stenophorida and a new order – Velocida which itself was created for Urosporoidea superfam. n. and Veloxidium . The third class was created – Squirmida – for Filipodium and Platyproteum . Thus, the eugregarines proved to be split and distributed among these three classes together with some other apicomplexans.

This point of view was challenged in 2017 by Simdyanov and co-authors, who performed the global integrated analysis of available morphological and molecular phylogenetic data and concluded that eugregarines are rather a monophyletic taxon. [13]

Several genera of gregarines are currently not classified: Acuta , Cephalolobus , Gregarina , Levinea , Menospora , Nematocystis , Nematopsis , Steinina , and Trichorhynchus .

Characteristics

The parasites are relatively large, spindle-shaped cells, compared to other apicomplexans and eukaryotes in general (some species are > 850 µm in length). Most gregarines have longitudinal epicytic folds (bundles of microtubules beneath the cell surface with nematode like bending behaviour): crenulations are instead found in the urosporidians.

Molecular biology

The gregarines are able to move and change direction along a surface through gliding motility without the use of cilia, flagella, or lamellipodia. [14] This is accomplished through the use of an actin and myosin complex. [15] The complexes require an actin cytoskeleton to perform their gliding motions. [16] In the proposed ‘capping’ model, an uncharacterized protein complex moves rearward, moving the parasites forward. [17]

History

The gregarines are among the oldest known parasites, having been described by the physician Francesco Redi in 1684. [18]

The first formal description was made by Dufour in 1828. He created the genus Gregarina and described Gregarina ovata from Folficula aricularia . He considered them to be parasitic worms. Koelliker recognised them as protozoa in 1848.

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.

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

Conoidasida is a class of parasitic alveolates in the phylum Apicomplexa. The class was defined in 1988 by Levine and contains two subclasses – the coccidia and the gregarines. All members of this class have a complete, hollow, truncated conoid. Gregarines tend to parasitize invertebrates with the mature gamonts being extracellular; the coccidia mostly infect vertebrates and have intracellular gamonts.

<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.

<span class="mw-page-title-main">Apicomplexan life cycle</span> Apicomplexa life cycle

Apicomplexans, a group of intracellular parasites, have life cycle stages that allow them to survive the wide variety of environments they are exposed to during their complex life cycle. Each stage in the life cycle of an apicomplexan organism is typified by a cellular variety with a distinct morphology and biochemistry.

Dactylosoma is a genus of parasitic alveolates of the phylum Apicomplexa.

The genus Schellackia comprises obligate unicellular eukaryotic parasites within the phylum Apicomplexa, and infects numerous species of lizards and amphibians worldwide. Schellackia is transmitted via insect vectors, primarily mites and mosquitoes, which take up the parasite in blood meals. These vectors then subsequently infect reptilian and amphibian which consume the infected insects. The parasites deform erythrocytes of the host into crescents, and can be visualized using a blood smear.

The Archigregarinorida are an order of parasitic alveolates in the phylum Apicomplexa. Species in this order infect marine invertebrates — usually annelids, ascidians, hemichordates and sipunculids.

The Neogregarinorida are an order of parasitic alveolates in the phylum Apicomplexa. Species in this order infect insects and are usually found in the fat body, hemolymph, hypodermis, intestine or Malpighian tubules. The most common site of infection is the fat body: many species are pathogenic for their hosts.

The Eugregarinorida are the most large and diverse order of gregarines — parasitic protists belonging to the phylum Apicomplexa. Eugregarines are found in marine, freshwater and terrestrial habitats. These species possess large trophozoites that are significantly different in morphology and behavior from the sporozoites. This taxon contains most of the known gregarine species.

The Caulleryellidae are a family of parasites in the phylum Apicomplexa. Species in this family mostly infect dipteran larvae.

The Schizocystidae are a family of parasitic alveolates in the phylum Apicomplexa. Species in this family infect insects.

A mucron is an attachment organelle found in archigregarines - an order of epicellular parasitic Conoidasida.

Filipodium is a genus of parasites in the phylum Apicomplexa. Species in this genus infect marine invertebrates.

Selenidium is a genus of parasitic alveolates in the phylum Apicomplexa. Species in this genus infect marine invertebrates.

Stylocephaloidea is a superfamily of parasites of the phylum Apicomplexia.

Syncystis is a genus of parasitic alveolates in the phylum Apicomplexa.

Schizocystidae is a genus of parasitic alveolates in the phylum Apicomplexa.

Nematopsis (Nee-mah-top-cis) is a genus gregarine Apicomplexan of the family Porosporidae. It is an aquatic parasite of crustaceans with a molluscan intermediate host. Nematopsis has been distinguished from the similar genus Porospora by its resistant and encapsulated oocyst. Little molecular biology has been performed on the members of the Nemaptosis and species are described based on molluscan and crustacean hosts as well as oocyst structure. A total of 38 species have been described and are found all over the world.

<i>Gregarina garnhami</i> Insect-parasitic micro-organism

Gregarina garnhami is a eukaryotic unicellular organism belonging to the Apicomplexa described in 1956 by Canning as a parasite found in several locusts, such as the desert locust, African migratory locust, and Egyptian locust. Especially, the desert locust is the host for this species, as up to 100% of animals can become infected. An estimated thousands of different species of gregarines can be in insects and 99% of these gregarines still need to be described. Each insect is said to host multiple species. A remarkable feature of G. garnhami is its autofluorescence.

Urospora is a genus of apicomplexan gregarines.

References

  1. ↑ Carreno RA, Martin DS, Barta JR (November 1999). "Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences". Parasitol. Res. 85 (11): 899–904. doi:10.1007/s004360050655. PMID   10540950. Archived from the original on 2001-03-20.
  2. ↑ Ménard R (February 2001). "Gliding motility and cell invasion by Apicomplexa: insights from the Plasmodium sporozoite". Cell. Microbiol. 3 (2): 63–73. doi: 10.1046/j.1462-5822.2001.00097.x . PMID   11207621.
  3. ↑ Meissner M, Schlüter D, Soldati D (October 2002). "Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion". Science. 298 (5594): 837–40. Bibcode:2002Sci...298..837M. doi:10.1126/science.1074553. PMID   12399593.
  4. ↑ Valigurová, Andrea; Koudela, Břetislav (August 2008). "Morphological analysis of the cellular interactions between the eugregarine Gregarina garnhami (Apicomplexa) and the epithelium of its host, the desert locust Schistocerca gregaria". European Journal of Protistology. 44 (3): 197–207. doi:10.1016/j.ejop.2007.11.006. PMID   18304787.
  5. ↑ Lange, C.E.; Lord, J.C. (2012). Insect Pathology - 2nd Edition (2nd ed.). Elsevier/Academic Press. pp. 367–387. ISBN   9780123849847.
  6. ↑ Cox, FE (December 1994). "The evolutionary expansion of the Sporozoa". International Journal for Parasitology. 24 (8): 1301–16. doi:10.1016/0020-7519(94)90197-x. PMID   7729983.
  7. ↑ Alarcón M E., Huang C-G, Tsai Y-S, Chen W-J, Kumar A (2011) Life cycle and morphology of Steinina ctenocephali (Ross 1909) comb. nov. (Eugregarinorida: Actinocephalidae), a gregarine of Ctenocephalides felis (Siphonaptera: Pulicidae) in Taiwan. Zoological Studies 50(6): 763-772
  8. ↑ Grassé, P.P.; Caullery, M.C. (1953). Traité de zoologie: anatomie, systématique, biologie. Tome I, Fasc. II, Protozaires, rhizopodes, Actinopodes, Sporozoaires, Cnidosporidies. Paris: Masson et Cie. OCLC   642231286.
  9. 1 2 Perkins FO, Barta JR, Clopton RE, Peirce MA, Upton SJ (2000). "Phylum Apicomplexa". In Lee JJ, Leedale GF, Bradbury P (eds.). An Illustrated guide to the Protozoa: organisms traditionally referred to as protozoa, or newly discovered groups. Vol. 1 (2nd ed.). Society of Protozoologists. pp. 190–369. ISBN   978-1891276224. OCLC   704052757.
  10. ↑ Leander BS (February 2008). "Marine gregarines: evolutionary prelude to the apicomplexan radiation?". Trends Parasitol. 24 (2): 60–7. doi:10.1016/j.pt.2007.11.005. PMID   18226585.
  11. ↑ Cavalier-Smith T (2014). "Gregarine site-heterogeneous 18S rDNA trees, revision of gregarine higher classification, and the evolutionary diversification of Sporozoa". Eur. J. Protistol. 50 (5): 472–495. doi:10.1016/j.ejop.2014.07.002. PMID   25238406.
  12. ↑ Adl SM, Simpson AG, Lane CE, Lukeš J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, Le Gall L, Lynn DH, McManus H, Mitchell EA, Mozley-Stanridge SE, Parfrey LW, Pawlowski J, Rueckert S, Shadwick L, Shadwick L, Schoch CL, Smirnov A, Spiegel FW (2012). "The revised classification of eukaryotes". J. Eukaryot. Microbiol. 59 (5): 429–93. doi:10.1111/j.1550-7408.2012.00644.x. PMC   3483872 . PMID   23020233.
  13. ↑ Simdyanov TG, Guillou L, Diakin AY, Mikhailov KV, Schrével J, Aleoshin VV (2017). "A new view on the morphology and phylogeny of eugregarines suggested by the evidence from the gregarine Ancora sagittata (Leuckart, 1860) Labbé, 1899 (Apicomplexa: Eugregarinida)". PeerJ. 5: e3354. doi: 10.7717/peerj.3354 . PMC   5452951 . PMID   28584702.
  14. ↑ Walker MH, Mackenzie C, Bainbridge SP, Orme C (November 1979). "A study of the structure and gliding movement of Gregarina garnhami". J Protozool. 26 (4): 566–574. doi:10.1111/j.1550-7408.1979.tb04197.x.
  15. ↑ Heintzelman MB (June 2004). "Actin and myosin in Gregarina polymorpha". Cell Motil. Cytoskeleton. 58 (2): 83–95. doi:10.1002/cm.10178. PMID   15083530.
  16. ↑ Mitchison TJ, Cramer LP (February 1996). "Actin-based cell motility and cell locomotion". Cell. 84 (3): 371–9. doi: 10.1016/s0092-8674(00)81281-7 . PMID   8608590.
  17. ↑ Sibley LD, Hâkansson S, Carruthers VB (January 1998). "Gliding motility: an efficient mechanism for cell penetration". Curr. Biol. 8 (1): R12–4. doi: 10.1016/S0960-9822(98)70008-9 . PMID   9427622.
  18. ↑ Redi, F (1684). Osservazioni intorno agli animali viventi, che si trovano negli animali viventi. Firenze: P. Matini. OCLC   8705660.

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