Eugregarinorida

Spore of Lithocystis minchinii, from Goodrich (1929).

Belongs within: Sporozoa.

The Eugregarinorida are a major subgroup of the gregarine parasites, found in a wide range of invertebrate hosts.

Let’s you and me enter syzygy
Published 9 May 2015

Finally, you and your beloved are together. For the two of you, there are no others; all the world is yours alone. You gaze into each other’s eyes, and then you pull your beloved into an embrace. Your lips touch in a passionate kiss. Your arms and legs intertwine in a firm hold. As you press so close to one another, it almost feels like you can no longer tell where the dividing line is between you. The excitement builds, and then… the two of you explode, each dissolving into a cascading avalanche of twitching gobbets of flesh.

Life cycle of Lecudina, from Clopton (2002).

This, roughly, is syzygy, a key event in the life cycle of many of the invertebrate-gut-parasitising protists known as eugregarines. Originally, the term ‘syzygy’ referred to the conjunction of two heavenly bodies, and provides a very poetic label for the process by which two of these unicellular organisms conjoin, rotating around one another as they produce an outer membrane to contain themselves within a single gametocyst. Once within the gametocyst, each divides into numerous gametes (which are produced through straight mitotic division, as eugregarines are haploid at maturity rather than diploid like ourselves). The resulting gametes will then be released from the gametocyst to fuse with one another in the production of diploid zygotes. Each zygote encloses itself in a resistant oocyst, in which state it may be passed out of the host’s digestive system and be swallowed by a new host. While within the oocyst, the zygote divides to produce a number of new haploid individuals. Once the oocyst is in a suitable host, the new eugregarines are released, ready to feed and hopefully to eventually find a syzygy of their own.

Mature individuals of Blabericola in association, copyright R. E. Clopton.

Eugregarines are part of the group of protists known as gregarines. They differ from the other two major subgroups of gregarines, the archigregarines and neogregarines, in that they do not include an extensive asexually reproducing phase in their life cycle in addition to the sexual phase. All known eugregarines are parasites of invertebrates: their hosts include arthropods, molluscs, annelids and tunicates. Most eugregarines parasitise only a single host species over the course of their life cycle. The only known exception is members of the family Porosporidae, which are believed to spend part of their life cycle in a crustacean, and part in a mollusc. However, the porosporid life cycle has only been observed in its entirety once in 1940, when H. F. Prytherch fed infective spores from an oyster to crabs. It has been suggested that Prytherch may have conflated two separate parasites, with the eugregarine infection observed in the crabs after feeding them the spores actually representing a pre-existing infection that they had been carrying before the start of the experiment (Clopton 2002).

Individual of Schneideria quadrinotatus, from Clopton (2002); scale bar = 100 µm. Offhand, I can’t be the only one who can’t help seeing the nuclei in these sort of drawings as eyes. And for some reason, they always seem to look a bit wistful.

The eugregarines are usually divided between three suborders. Two of these, the Septatorina and Aseptatorina, include the great majority of species and are distinguished (as their names suggest) by the presence or absence of septae dividing the cell into sections. The third suborder includes the single small genus Siedlickia, parasites of marine annelids, which differs from other eugregarines in that it does not go through syzygy; instead, reproductive cells are budded directly off the mature feeding cells. The relationships between the three suborders are largely unknown; the Aseptatorina in particular seems to be defined largely by plesiomorphies. Clopton (2009) argued for a marine ancestry of eugregarines as a whole, and that the radiation of the septate eugregarines had been driven by adaptations of the gametocyst allowing their transmission in freshwater and terrestrial habitats. However, both the aseptate and septate eugregarines include parasites of marine, freshwater and terrestrial hosts. The fact that Clopton did not refer in 2009 to the marine members of the Septatorina (in the Porosporidae and various families of the Gregarinoidea) is somewhat bemusing as he himself had reviewed them some years earlier in his 2002 chapter on the eugregarines for The Illustrated Guide to the Protozoa. It is possible that he simply assumed the marine species to sit outside the terrestrial-freshwater clade, but it would have been nice for him to say so.

Multiple syzygy in Hyalospora roscoviana, from Clopton (2002). The one in front doesn’t look like it was quite expecting this.

Ignorance of the marine eugregarines does seem to be a theme, though: they’re definitely less well-studied than the parasites of terrestrial species. Not that the latter can claim to have been exhaustively studied either: as noted by Clopton (2002), while over 1600 species of eugregarine have been described, only a fraction (much less than one percent) of potential hosts have been investigated for their presence. As almost every investigation of a new host results in the description of new parasite species, it is possible that the total number of eugregarine species out there ranks in the millions. Eugregarines are morphologically and behaviourally diverse. Attachment to the cells of the host’s intestinal lining is via a structure called the epimerite, which may be a simple nubbin or may be a complex branching, fingered, collared or dart-like structure. When not attached to the host cell, most eugregarines move by gliding, but the worm-like Selenidiidae move by nondirectional swinging or thrashing. Many taxa are all distinguished by the characteristics of their syzygy. They may connect end to end, or they may lie top-to-tail. Members of the septate superfamily Gregarinoidea form associations some time before entering actual syzygy, so they are often found connected (whereas other taxa that do not become conjoined until the point of syzygy are more often found as isolated cells). Syzygy is most often between two individuals, but some Gregarinoidea regularly form associations of three or more. At least one species, Hirmocystis polymorpha, has been found in head-to-tail chains of up to twelve individuals. Whether such polygamous associations lead to all the individuals involved combining to form one gametocyst, or whether some form of competition occurs to whittle them down to a single victorious pair, is something I haven’t yet discovered.

Systematics of Eugregarinorida

Characters (from Adl et al. 2019): Trophozoite with epimerite in gregarines with septum or mucron in gregarines without septum; syzygy followed by encystment of gamonts; oocysts with eight sporozoites.

<==Eugregarinorida
    |--Diplocystis Künstler 1887 non Berkeley & Curtis 1869 (ICBN) [Diplocystidae, Haplocyta, Homoplaridea]D49
    |    |--D. clerckiD49
    |    |--D. oxycani Dumbleton 1949D49
    |    |--D. phryganeaeD49
    |    `--D. schneideriD49
    `--UrosporidaeBK77
         |--Gonospora mercieri (see below for synonymy)BK77
         |--Diplodina gonadiperthaBK77
         |--CystobiaBK77
         |    |--C. holothuriae (Schneider 1858) [=Gregarina holothuriae]BK77
         |    |--C. irregularis (Minchin 1893) [=Gregarina irregularis, Diplodina irregularis, Gonospora irregularis]BK77
         |    `--C. stichopiBK77
         |--UrosporaBK77
         |    |--U. chiridotae (Dogiel 1906) [=Cystobia chiridotae]BK77
         |    |--U. echinocardiiBK77
         |    |--U. neapolitanaBK77
         |    `--U. synaptae (Cuénot 1891) [=Syncystis synaptae]BK77
         `--LithocystisBK77
              |--L. brachycercusBK77
              |--L. cucumariaeBK77
              |--L. foliaceaBK77
              |--L. microsporaBK77
              |--L. minchinii (Woodcock 1904) [=Cystobia minchinii, Diplodina minchinii]BK77
              `--L. schneideriBK77
Eugregarinorida incertae sedis:
  Actinocephalus megabuniCM07
  AnthorhynchusCM07
    |--A. longisporaCM07
    `--A. sophiaeCM07
  Arachnocystis arachnoideaCM07
  Contospora opalniaeCM07
  Cosmetophilus vononesCM07
  DoliosporaCM07
    |--D. repeliniCM07
    `--D. troguliCM07
  Echinoocysta phalangiiCM07
  SciadiophoraCM07
    |--S. caudataCM07
    |--S. claviformisCM07
    |--S. fissidensCM07
    |--S. gagrellulaCM07
    |--S. geronowitschiCM07
    `--S. phalangiiCM07
  Leidyana migratorAS12, LCK03
  GregarinaAS12
    |--G. cuneataLCK03
    |--G. niphandrodesLCK03
    |--G. ovataRK91
    |--G. polymorphaLCK03
    `--G. steiniLCK03
  AmoebogregarinaAS12
  Ascogregarina armigereiAS12, SM10
  BlabericolaAS12
  CephaloidophoraAS12
  ColepismatophilaAS12
  DifficilinaAS12
  GanymedesAS12
  GeneiorhynchusAS12
  HeliosporaAS12
  LecudinaAS12
  NeoasterophoraAS12
  ParaschneideriaAS12
  PrismatosporaAS12
  ProtomagalhaensiaAS12
  PsychodiellaAS12
  PyxiniaAS12
  StylocephalusAS12
  ThiriotiaAS12
  TrichotokaraAS12
  XiphocephalusAS12
  ApolocystisAB19
  AncoraAB19
  CaliculiumAB19
  CystocephalusAB19
  DiplauxisAB19
  EnterocystisAB19
  HentscheliaAB19
  HirmocystisAB19
  MonocystellaAB19
  Monocystis Stein 1848AB19, R74
    |--M. agilisLCK03
    |--M. krin Righi 1974R74
    |--M. minor Boisson 1957R74
    |--M. naidis Voss 1921R74
    |--M. octavi Righi 1974R74
    |--M. perichaeta (Beddard 1888)R74
    |--M. pontodrili Subbarao et al. 1979B07
    |--M. rostrata Mulsow 1911R74
    `--M. tupi Righi 1974R74
  NematopsisAB19
  NematocystisAB19
  ParalecudinaAB19
  PileocephalusAB19
  PolyplicariumAB19
  PolyrhabdinaAB19
  PorosporaAB19
  PyxinioidesAB19
  SphaerorhynchusAB19
  SteininaAB19
  StenophoraAB19
  SyciaAB19
  ThalicolaAB19
  UradiophoraAB19
  ZygosomaAB19

Gonospora mercieri [incl. Lithocystis muelleri Giard 1886, Syncystis muelleri, Urospora muelleri, Esarabdina synaptae Mingazzini 1891]BK77

*Type species of generic name indicated

References

[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.

[BK77] Barel, C. D. N., & P. G. N. Kramers. 1977. A survey of the echinoderm associates of the north-east Atlantic area. Zoologische Verhandelingen 156: 1–159.

[B07] Blakemore, R. J. 2007. Origin and means of dispersal of cosmopolitan Pontodrilus litoralis (Oligochaeta: Megascolecidae). European Journal of Soil Biology 43: S3–S8.

Clopton, R. E. 2002. Order Eugregarinorida Léger, 1900. In: Lee, J. J., G. Leedale, D. Patterson & P. C. Bradbury (eds) Illustrated Guide to the Protozoa, 2nd ed., vol. 1 pp. 205–288. Society of Protozoologists: Lawrence (Kansas).

Clopton, R. E. 2009. Phylogenetic relationships, evolution, and systematic revision of the septate gregarines (Apicomplexa: Eugregarinorida: Septatorina). Comp. Parasitol. 76 (2): 167–190.

[CM07] Cokendolpher, J. C., & P. G. Mitov. 2007. Natural enemies. In: Pinto-da-Rocha, R., G. Machado & G. Giribet (eds) Harvestmen: The Biology of Opiliones pp. 339–373. Harvard University Press: Cambridge (Massachusetts).

[D49] Dumbleton, L. J. 1949. Diplocystis oxycani n.sp.—a gregarine parasite of Oxycanus cervinatus Walk. Transactions and Proceedings of the Royal Society of New Zealand 77 (4): 530–532.

[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.

[RK91] Rentz, D. C. F., & D. K. McE. Kevan. 1991. Dermaptera (earwigs). In: CSIRO. The Insects of Australia: A textbook for students and research workers 2nd ed. vol. 1 pp. 360–368. Melbourne University Press: Carlton (Victoria).

[R74] Righi, G. 1974. Alguns Sporozoa (Gregarinida e Haplosporida) de Oligochaeta (Naididae e Enchytraeidae) brasileiros. Papéis Avulsos de Zoologia 28 (11): 185–195.

[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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