Illustration of Cryptosporidium parvum sporozoites emerging from oocysts, from here.

Belongs within: Myzozoa.
Contains: Aconoidasida, Eimeriorina, Adeleorina, Eugregarinorida.

The Sporozoa is a group of unicellular organisms parasitic on animals, characterised by the presence of an apical complex at one end of the cell containing organelles (rhoptries and micronemes) that secrete enzymes used in piercing the membrane of host cells. In sporozoans other than the Aconoidasida, the apical complex is tipped by a funnel of microtubules called the conoid. The Sporozoa are also commonly referred to as the Apicomplexa, though Cavalier-Smith & Chao (2004) used the latter name to refer to a larger clade also including the related organisms Colpodella and Acrocoelus.

Of gregarines
Published 2 February 2009
An assortment of lecudinid eugregarines. The front end of the cell is towards the lower left in each individual. Image from Leander (2007) via Brian S. Leander.

The Sporozoa are perhaps the most famous group of protozoan parasites. As well as being one of the few protozoan groups distinctive enough to be well-characterised prior to the advent of electron microscopy and molecular analysis (albeit with a few hangers-on such as microsporidians and myxozoans that have since been cast aside from the sporozoan community), distinguished by their lack of motile organelles and intracellular invasion of their hosts, sporozoans include the causative agents of such maladies as malaria and toxoplasmosis. In many references, you may find the Sporozoa referred to as Apicomplexa, a name that refers to the apical complex, an organelle at the front end of the cell that is used to invade the cells of the sporozoan’s host. However, as the apical complex is also found in some flagellates that are closely related to sporozoans (such as Colpodella), the name Apicomplexa is better used for the larger clade including these taxa while the name Sporozoa is restricted to the nested aflagellate clade (Cavalier-Smith & Chao 2004).

Sporozoans have been divided into three classes, the invertebrate parasites Gregarinae (or Gregarinea), Coccidia (intestinal parasites of vertebrates) and Hematozoa (parasites of vertebrate blood cells). Phylogenetic analyses have indicated that the basal division in Sporozoa is between the vertebrate-parasitic Coccidia and Hematozoa on one branch (the Coccidiomorpha), and the Gregarinae on the other, though the Gregarinae is less well supported as monophyletic than the Coccidiomorpha and may yet be paraphyletic (Leander & Ramey 2006; Leander et al. 2006). One notable exception is that the vertebrate parasite Cryptosporidium, previously regarded as a coccidian, may in fact be related to the gregarines or even derived from within them. Not surprisingly, their choice of hosts means that the Coccidiomorpha are by far the better studied of the two clades, while the Gregarinae have kind of been the poor relation. Nevertheless, it is the gregarines that are my focus today.

Gregarines have been divided into three groups, the archigregarines, eugregarines and neogregarines (Leander 2007), but it seems more than likely that these represent a series of grades, with eugregarines paraphyletic to neogregarines and archigregarines paraphyletic to the eugregarine + neogregarine clade. In contrast to the complex life-cycles of some coccidiomorphs, gregarines have fairly simple life histories with only a single host. Transmission from one host to another is usually via oocysts released with the host faecal matter, but some gregarine oocysts hitch a ride with their host’s gametes during copulation as protozoan STDs. Once inside the host, the oocysts hatch out into infective sporozoites that attach to or invade host cells and develop into feeding trophozoites. Some gregarines can reproduce asexually; the majority cannot. Sexual reproduction occurs by two trophozoites joining together as reproductive gamonts and becoming enclosed within a gametocyst; within the gametocyst they will each divide into hundreds of gametes that will fuse to form oocysts, ready for release.

Selenidium sp., showing the wriggling movement, from Leander (2007).

As I said before, the “archigregarines” probably represent the basal grade of gregarines. They are all intestinal parasites of marine invertebrates, and as such have been unfairly condemned as of little interest to anyone. Archigregarines have very similar sporozoites and trophozoites that are vermiform (worm-shaped) and generally move by wriggling (go here for videos of gregarine movement). Some archigregarines have cells with numerous longitudinal folds, others are smooth. Archigregarines also retain the ancestral characteristic of feeding on their host by using their apical complex to pierce the host cell and sucking out its contents.

The ‘eugregarines’ include the majority of gregarines (at least, the majority of described gregarines), and include parasites of freshwater and terrestrial as well as marine invertebrates. Again, their study has been biased towards those species that are parasites of insects, with the remainder being generally snubbed. Most marine eugregarines have been lumped together as the genus ‘Lecudina‘, with little to unite them other than that they are marine eugregarines (Leander 2007). Eugregarines differ from archigregarines in having morphologically quite distinct sporozoites and trophozoites. Their cell walls also became very rigid, and they lost the wriggling ability of archigregarines. Instead, eugregarines developed a system of gliding motility, with an actinomyosin skeleton running along the edge of the numerous surface folds. Ancestrally, eugregarines are intestinal parasites like archigregarines, but instead of the active feeding process of eugregarines, eugregarines absorb nutrients from the host through micropores on the cell surface (Leander et al. 2006).

Two conjoined gamonts of the polychaete coelom parasite Pterospora floridiensis, from Leander (2007).

Neogregarines are a derived subgroup of eugregarines with reduced trophozoites that specialise on terrestrial hosts (mostly insects) and mostly live in non-intestinal tissues. Another group of eugregarines, the urosporidians, became parasites of their host’s coelom. Urosporidians lost their direct attachment to host cells, and became free-floating within the tissue as united gamont pairs. The gliding motility and longitudinal folds of other eugregarines were lost, and instead urosporidians move by pulsations of the cell walls. Cells became branched—many are V-shaped with two primary branches that each divide distally into a number of smaller “fingers”.

Archigregarines in particular retain a number of features that are believed to be ancestral for sporozoans as a whole (such as sucking feeding), and Leander et al. (2006) suggest that they may constitute the ancestral group not just for eugregarines, but also for coccidiomorphs and hence sporozoans as a whole. Interestingly, gregarines (including archigregarines), so far as is known, lack the residual plastid found in coccidiomorphs. It is currently a subject of some debate as to whether the sporozoan (really coccidiomorph) plastid is homologous with that found in the related dinoflagellates or not (see here for an earlier take of mine on the issue), and the position of the plastid-less ‘archigregarines’ could have significant implications for this debate.

Systematics of Sporozoa

Characters (from Adl et al. 2012, as Apicomplexa): At least one stage of the life cycle with flattened sub-pellicular vesicles and apical complex consisting of one or more polar rings, rhoptries, micronemes, conoid, and sub-pellicular microtubules; sexuality, where known, by syngamy followed by immediate meiosis to produce haploid progeny; asexual reproduction of haploid stages occurring by binary fission, endodyogeny, endopolyogeny, and/or schizogony; locomotion by gliding, body flexion, longitudinal ridges, and/or cilia; parasitic.

<==Sporozoa [Coccidea, Coccidiida, Coccidiomorpha, Coccidiomorphina, Conoidasida, Euspora, Polannulifera, Telosporidia]
    |    |--AconoidasidaSM10
    |    `--CoccidiaAS12
    |         |  i. s.: Aggregata Frenzel 1885K92, AB19
    |         |           `--A. eberthiK92
    |         |--EimeriorinaSM10
    |         `--AdeleorinaAS12
    `--Gregarinasina [Gregarinae, Gregarinasina, Gregarinea, Gregarinia, Gregarinomorpha, Gregarinomorphea]AB19
         |  i. s.: AcutaAS12
         |         CephalolobusAS12
         |         LevineaAS12
         |         MenosporaAS12
         |         TrichorhynchusAS12
         |         ZygocystisC79
         |         Digyalum Koura et al. 1990AB19
         |         Exoschizon Hukui 1939AB19
         |--+--Cryptosporidium [Cryptogregaria, Cryptogregarinorida]C-SC04
         |  |    |  i. s.: C. felisN00
         |  |    |         C. meleagridisMM03
         |  |    |--+--C. serpentisSM10
         |  |    |  `--C. murisSM10
         |  |    `--+--C. parvumSM10
         |  |       `--+--C. baileyiSM10
         |  |          `--C. wrairiC-SC04
         |  `--ArchigregarinoridaAB19
         |       |  i. s.: MeroselenidiumAB19
         |       |         MerogregarinaAB19
         |       |         SelenocystisAB19
         |       |--SquirmideaC-S18
         |       |    |--FilipodiumAB19
         |       |    `--PlatyproteumC-S18
         |       `--ParagregareaC-S18
         |            |--VeloxidiumAS12
         |            `--SelenidiumSM10
         |                 |--S. terebellaeC-SM10
         |                 `--S. vivaxC-S04
            |    |--GemmocystisAS12
            |    `--Rhytidocystis [Histogregaria]SM10
            |         `--R. polygordiaeSM10
                      |--Ophriocystis eletroscirrhaLCK03
                      |--Mattesia geminataC-S04
Sporozoa incertae sedis:
  Akiba cauleryiK92
  Babesiosoma stableriK92
  Trophosphaera Le Calvez 1939AB19
    `--T. planorbulinaeLT64
  Christalloidophora Dehome 1934AB19
  Dobellia Ikeda 1914AB19
  Echinococcidium Porchet 1978AB19
  Globidiellum Brumpt 1913AB19
  Joyeuxella Brasil 1902AB19
  Rhabdospora Laguesse 1906 non (Durieu & Mont. ex Sacc.) Sacc. 1884 (ICBN)AB19
  Spermatobium Eisen 1895AB19
  Spiriopsis Arvy & Peters 1972AB19
  Spirogregarina Wood & Herman 1943AB19
  Toxocystis Léger & Duboscq 1910AB19
  Chitonicium simplexBRW98

*Type species of generic name indicated


[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

[BRW98] Beesley, P. L., G. J. B. Ross & A. Wells (eds) 1998. Fauna of Australia vol. 5. Mollusca: The Southern Synthesis. Part A. Australian Biological Resources Study: Canberra.

[C-S18] Cavalier-Smith, T. 2018. Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences. Protoplasma 255: 297–357.

[C-SC04] Cavalier-Smith, T., & E. E. Chao. 2004. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.) European Journal of Protistology 40: 185–212.

[C79] Curds, C. R. 1979. Group phenomena in the phylum Protozoa. In: Larwood, G., & B. R. Rosen (eds) Biology and Systematics of Colonial Organisms pp. 29–37. Academic Press: London.

[K92] Krylov, M. V. 1992. The origin of heteroxeny in Sporozoa. Parazitologiya 26 (5): 361–368.

Leander, B. S. 2007. Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends in Parasitology 24 (2): 60–67.

[LCK03] Leander, B. S., R. E. Clopton & P. J. Keeling. 2003. Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and β-tubulin. International Journal of Systematic and Evolutionary Microbiology 53: 345–354.

Leander, B. S., S. A. J. Lloyd, W. Marshall & S. C. Landers. 2006. Phylogeny of marine gregarines (Apicomplexa)—Pterospora, Lithocystis and Lankesteria—and the origin(s) of coelomic parasitism. Protist 157: 45–60.

Leander, B. S., & P. A. Ramey. 2006. Cellular identity of a novel small subunit rDNA sequence clade of apicomplexans: description of the marine parasite Rhytidocystis polygordiae n. sp. (host: Polygordius sp., Polychaeta). Journal of Eukaryotic Microbiology 53 (4): 280–291.

[LT64] Loeblich, A. R., Jr & H. Tappan. 1964. Sarcodina: chiefly “thecamoebians” and Foraminiferida. In: Moore, R. C. (ed.) Treatise on Invertebrate Paleontology pt C. Protista 2 vol. 1. The Geological Society of America and The University of Kansas Press.

[MM03] Mallon, M., A. MacLeod, J. Wastling, H. Smith, B. Reilly & A. Tait. 2003. Population structures and the role of genetic exchange in the zoonotic parasite Cryptosporidium parvum. Journal of Molecular Evolution 56: 407–417.

[N00] Nichols, G. L. 2000. Food-borne protozoa. British Medical Bulletin 56 (1): 209–235.

[SM10] Saffo, M. B., A. M. McCoy, C. Rieken & C. H. Slamovits. 2010. Nephromyces, a beneficial apicomplexan symbiont in marine animals. Proceedings of the National Academy of Sciences of the USA 107 (37): 16190–16195.

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