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Perkinsea

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Perkinsea
Double infection of two late Dinovorax pyriformis trophonts in a Prorocentrum micans cell. Scale bar: 10 μm.
Scientific classification Edit this classification
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Myzozoa
Subphylum: Dinozoa
Infraphylum: Perkinsozoa
Norén & Moestrup 1999[2]
Class: Perkinsea
Levine 1978[1]
Clades
Synonyms
  • Perkinsasida
  • Perkinsorida
  • Perkinsemorphina

Perkinsids are single-celled protists that live as intracellular parasites of a variety of other organisms. They are classified as the class Perkinsea within the monotypic phylum Perkinsozoa. It is part of the eukaryotic supergroup Alveolata, along with dinoflagellates, their closest relatives, and another parasitic group known as Apicomplexa. Perkinsids are found in aquatic environments, as parasites of dinoflagellates and various animals.

Description

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All known Perkinsozoa are intracellular parasites of a range of organisms, particularly microalgae and animals.[3] Species of Parviluciferaceae, Pararosariidae and Maranthos are parasites of dinoflagellates.[4][5] Rastrimonas parasitize cryptophyte algae.[5] Xcellidae, Perkinsidae and Acrocoelus are parasites of various animals: fish,[6] bivalve molluscs[7] and acorn worms, respectively.[8] Perkinsozoa are found in aquatic environments, both marine[2] and freshwater.[9]

Systematics

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Taxonomic history

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Perkinsids were first described by Norman D. Levine in 1978, as the class Perkinsea within Alveolata. Levine only included one genus, Perkinsus, described in the same publication.[1] Later, the same author treated this group as class Perkinsasida within the phylum Apicomplexa, suggesting that Perkinsus is the most primitive apicomplexan.[10] However, this placement was controversial, and was later disproven by phylogenetic analyses that proved more evolutionary proximity to dinoflagellates than to apicomplexans.[11]

In 1999, with the discovery of Parvilucifera, biologists Fredrik Norén and Øjvind Moestrup separated the class Perkinsea into a new phylum Perkinsozoa, within the Alveolata, to accommodate these two genera.[2] In 2002 a third genus was described, Cryptophagus (now renamed Rastrimonas), but it was never genetically sequenced, which makes its phylogenetic position uncertain.[12]

In 2014 a new class was added to the phylum, known as Squirmidea.[13] However, phylogenetic analyses later demonstrated that squirmids are more closely related to the clade uniting Apicomplexa and Colpodellida than to dinoflagellates and perkinsids, and its status as a class of Perkinsozoa was rejected, making Perkinsea the only remaining class.[14][15]

Phylogeny

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Colponemids

Simplified cladogram of Alveolata based on 2023 phylogenomic analyses.[14][15]

Perkinsids are a monophyletic group (or clade) of Alveolata, a large group of ecologically diverse protists such as dinoflagellates, ciliates, apicomplexans and chrompodellids, all characterized by the presence of cortical alveoli below their cell membrane. In particular, perkinsids are the sister group of dinoflagellates, together forming a clade known as Dinozoa.[16] Both groups, along with apicomplexans and their closest relatives, compose a clade known as Myzozoa.[14][15]

Classification

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As of 2023, the order-level classification of perkinsids remains ambiguous, and orders are very sparsely used. The families Pararosariidae and Parviluciferaceae have no assigned parent order,[4][5] although one author, Thomas Cavalier-Smith, previously placed Parvilucifera within the order Rastrimonadida, along with Rastrimonas.[17] This has not been supported by any other author, and both Rastrimonadida and Rastrimonas are omitted from current classifications for lacking molecular data.[12] Similarly, the genus Acrocoelus, assigned directly to the order Acrocoelida without a family,[17] is also excluded due to the absence of molecular data.[18] The genus Maranthos, although genetically sequenced, is not assigned to any family or order.[19] The remaining groups, Perkinsidae and Xcellidae, are only sometimes assigned to order Perkinsida,[20][21] while in other instances their parent taxon is directly Perkinsea.[6][22] Taxonomic ranks (i.e. families, orders, classes...) are mostly omitted in favour of using only clades.[18] Shown below is the commonly accepted scheme, omitting order-level taxa:

Simplified cladogram of Perkinsea based on 2021-2023 phylogenetic analyses.[19][5][20] Environmental DNA clades are omitted, with the exception of clade 'NAG01' which groups possible infectious agents of tadpoles.[5]

As mentioned above, two genera have uncertain placement because they have never been genetically sequenced, but they have been assigned to Perkinsea on the basis of their morphology:[13]

References

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  1. ^ a b c d Norman D. Levine (1978). "Perkinsus gen. n. and Other New Taxa in the Protozoan Phylum Apicomplexa". The Journal of Parasitology. 64 (3): 549. doi:10.2307/3279807. JSTOR 3279807.
  2. ^ a b c d Norén, Fredrik; Moestrup, Øjvind; Rehnstam-Holm, Ann-Sofi (October 1999). "Parvilucifera infectans Norén et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae". European Journal of Protistology. 35 (3): 233–254. doi:10.1016/S0932-4739(99)80001-7.
  3. ^ Agostina V. Marano; Carmen L.A. Pires-Zottarelli; José I. de Souza; Sally L. Glocking; Eduardo Leaño; Claire M.M. Gachon; Martina Strittmatter; Frank H. Gleason (2012). "Chapter 11: Hyphochytriomycota, Oomycota and Perkinsozoa (Super-group Chromalveolata)". In E.B. Gareth Jones; Ka-Lai Pang (eds.). Marine Fungi and Fungal-like Organisms. Göttingen: De Gruyter. pp. 167–214. doi:10.1515/9783110264067.167. ISBN 978-3-11-026406-7.
  4. ^ a b c Albert Reñé; Elisabet Alacid; Isabel Ferrera; Esther Garcés (24 August 2017). "Evolutionary Trends of Perkinsozoa (Alveolata) Characters Based on Observations of Two New Genera of Parasitoids of dinoflagellates, Dinovorax gen. nov. and Snorkelia gen. nov". Frontiers in Microbiology. 8: 1863. doi:10.3389/FMICB.2017.01863. ISSN 1664-302X. PMC 5609580. PMID 28970818. Wikidata Q42163896.
  5. ^ a b c d e f Boo Seong Jeon; Myung Gil Park (29 November 2021). "A Novel Parasitoid of Marine Dinoflagellates, Pararosarium dinoexitiosum gen. et sp. nov. (Perkinsozoa, Alveolata), Showing Characteristic Beaded Sporocytes". Frontiers in Microbiology. 12: 748092. doi:10.3389/FMICB.2021.748092. ISSN 1664-302X. PMC 8667275. PMID 34912310. Wikidata Q112637999.
  6. ^ a b c d Mark A Freeman; Janina Fuss; Árni Kristmundsson; et al. (13 May 2017). "X-Cells Are Globally Distributed, Genetically Divergent Fish Parasites Related to Perkinsids and Dinoflagellates". Current Biology. 27 (11): 1645-1651.e3. doi:10.1016/J.CUB.2017.04.045. ISSN 0960-9822. PMID 28528902. Wikidata Q36377210.
  7. ^ Villalba, A.; et al. (2004). "Perkinsosis in molluscs: a review" (PDF). Aquatic Living Resources. 17 (4): 411–32. doi:10.1051/alr:2004050.
  8. ^ a b Isabel Fernández; Fernando Pardos; Jesús Benito; Nina Larissa Arroyo (1999). "Acrocoelus glossobalani gen. nov. et sp. nov., a protistan flagellate from the gut of the enteropneust Glossabalanus minutus". European Journal of Protistology. 35 (1): 55–65. doi:10.1016/S0932-4739(99)80022-4.
  9. ^ Mangot, Jean-François; Debroas, Didier; Domaizon, Isabelle (16 May 2010). "Perkinsozoa, a well-known marine protozoan flagellate parasite group, newly identified in lacustrine systems: a review". Hydrobiologia. 659 (1): 37–48. doi:10.1007/s10750-010-0268-x. S2CID 36522615.
  10. ^ Norman D. Levine (1988). The Protozoan Phylum Apicomplexa. Vol. 1 (1 ed.). CRC Press. ISBN 9781315897004.
  11. ^ C. Louise Goggin; Stephen C. Barker (1993). "Phylogenetic position of the genus Perkinsus (Protista, Apicomplexa) based on small subunit ribosomal RNA". Molecular and Biochemical Parasitology. 60 (1): 65–70. doi:10.1016/0166-6851(93)90029-w. PMID 8366895.
  12. ^ a b Sarah Itoïz; Sebastian Metz; Evelyne Derelle; Albert Reñé; Esther Garcés; David Bass; Philippe Soudant; Aurélie Chambouvet (1 January 2021). "Emerging Parasitic Protists: The Case of Perkinsea". Frontiers in Microbiology. 12: 735815. doi:10.3389/FMICB.2021.735815. ISSN 1664-302X. PMC 8792838. PMID 35095782. Wikidata Q111321231.
  13. ^ a b Thomas Cavalier-Smith (30 July 2014). "Gregarine site-heterogeneous 18S rDNA trees, revision of gregarine higher classification, and the evolutionary diversification of Sporozoa". European Journal of Protistology. 50 (5): 472–495. doi:10.1016/J.EJOP.2014.07.002. ISSN 0932-4739. PMID 25238406. Wikidata Q39198055.
  14. ^ a b c Corey C. Holt; Elisabeth Hehenberger; Denis V. Tikhonenkov; Victoria K. L. Jacko-Reynolds; Noriko Okamoto; Elizabeth C. Cooney; Nicholas A. T. Irwin; Patrick J. Keeling (3 November 2023). "Multiple parallel origins of parasitic Marine Alveolates". Nature Communications. 14 (1): 7049. doi:10.1038/S41467-023-42807-0. ISSN 2041-1723. PMC 10624901. PMID 37923716. Wikidata Q125317501.
  15. ^ a b c Varsha Mathur; Eric D. Salomaki; Kevin C. Wakeman; Ina Na; Waldan K. Kwong; Martin Kolísko; Patrick John Keeling (4 January 2023). "Reconstruction of Plastid Proteomes of Apicomplexans and Close Relatives Reveals the Major Evolutionary Outcomes of Cryptic Plastids". Molecular Biology and Evolution. 40 (1): msad002. doi:10.1093/MOLBEV/MSAD002. ISSN 0737-4038. PMC 9847631. PMID 36610734. Wikidata Q124684358.
  16. ^ Thomas Cavalier-Smith (5 September 2017). "Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences". Protoplasma. 255 (1): 297–357. doi:10.1007/S00709-017-1147-3. ISSN 0033-183X. PMC 5756292. PMID 28875267. Wikidata Q47194626.
  17. ^ a b T. Cavalier-Smith; E.E. Chao (September 2004). "Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.)". European Journal of Protistology. 40 (3): 185–212. doi:10.1016/J.EJOP.2004.01.002. ISSN 0932-4739. Wikidata Q54540793.
  18. ^ a b Sina M. Adl; David Bass; Christopher E. Lane; et al. (1 January 2019). "Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes". Journal of Eukaryotic Microbiology. 66 (1): 4–119. doi:10.1111/JEU.12691. ISSN 1066-5234. PMC 6492006. PMID 30257078. Wikidata Q57086550.
  19. ^ a b c Albert Reñé; Elisabet Alacid; Rachele Gallisai; Aurelie Chambouvet; Alan D Fernández-Valero; Esther Garcés (5 August 2021). "New Perkinsea Parasitoids of Dinoflagellates Distantly Related to Parviluciferaceae Members". Frontiers in Microbiology. 12: 701196. doi:10.3389/FMICB.2021.701196. ISSN 1664-302X. PMC 8375308. PMID 34421856. Wikidata Q112639124.
  20. ^ a b c Clive W. Evans; Selina Patel; Nicholas J. Matzke; Craig D. Millar (28 April 2023). "Cryoxcellia borchgrevinki gen. nov., sp. nov., a new parasitic X‑cell species in an Antarctic nototheniid fish, the bald notothen Trematomus borchgrevinki". Polar Biology. 46: 513–521. doi:10.1007/S00300-023-03132-W. ISSN 0722-4060. Wikidata Q124515389.
  21. ^ a b c Egil Karlsbakk; Cecilie Flatnes Nystøyl; Heidrun Plarre; Are Nylund (28 August 2021). "A novel protist parasite, Salmoxcellia vastator n. gen., n. sp. (Xcelliidae, Perkinsozoa), infecting farmed salmonids in Norway". Parasites & Vectors. 14: 431. doi:10.1186/S13071-021-04886-0. ISSN 1756-3305. PMC 8400403. PMID 34454593. Wikidata Q124515368.
  22. ^ a b Thomas Desvignes; Henrik Lauridsen; Alejandro Valdivieso; et al. (15 July 2022). "A parasite outbreak in notothenioid fish in an Antarctic fjord". iScience. 25: 104588. doi:10.1016/J.ISCI.2022.104588. ISSN 2589-0042. Wikidata Q124515399.
  23. ^ Boo Seong Jeon; Myung Gil Park (21 December 2018). "Tuberlatum coatsi gen. n., sp. n. (Alveolata, Perkinsozoa), a New Parasitoid with Short Germ Tubes Infecting Marine Dinoflagellates". Protist. 170 (1): 82–103. doi:10.1016/J.PROTIS.2018.12.003. ISSN 1434-4610. PMID 30797136. Wikidata Q91851560.
  24. ^ Brugerolle, G. (2003). "Apicomplexan parasite Cryptophagus renamed Rastrimonas gen. nov". European Journal of Protistology. 39 (1): 101. doi:10.1078/0932-4739-00910.
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