Perkinsea

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Perkinsea
Dinovorax pyriformis PMC5609580 fig1c.png
Double infection of two late Dinovorax pyriformis trophonts in a Prorocentrum micans cell. Scale bar: 10 μm.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Myzozoa
Subphylum: Dinozoa
Infraphylum: Perkinsozoa
Norén & Moestrup 1999 [1]
Class: Perkinsea
Levine 1978 [2]
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.

Contents

Description

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 [1] and freshwater. [9]

Systematics

Taxonomic history

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. [2] 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. [1] 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

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

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]

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">Alveolate</span> Superphylum of protists

The alveolates are a group of protists, considered a major clade and superphylum within Eukarya. They are currently grouped with the stramenopiles and Rhizaria among the protists with tubulocristate mitochondria into the SAR supergroup.

Perkinsus marinus is a species of alveolate belonging to the phylum Perkinsozoa. It is similar to a dinoflagellate. It is known as a prevalent pathogen of oysters, causing massive mortality in oyster populations. The disease it causes is known as dermo or perkinsosis, and is characterized by the degradation of oyster tissues. The genome of this species has been sequenced.

Perkinsus is a genus of alveolates in the phylum Perkinsozoa. The genus was erected in 1978 to better treat its type species, Perkinsus marinus, known formerly as Dermocystidium marinum. These are parasitic protozoans that infect molluscs, at least some of which cause disease and mass mortality. P. marinus is the most notorious, causing the disease perkinsosis, or dermo, in wild and farmed oysters.

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

Colpodella is a genus of alveolates comprising 5 species, and two further possible species: They share all the synapomorphies of apicomplexans, but are free-living, rather than parasitic. Many members of this genus were previously assigned to a different genus - Spiromonas.

Chromera velia, also known as a "chromerid", is a unicellular photosynthetic organism in the superphylum Alveolata. It is of interest in the study of apicomplexan parasites, specifically their evolution and accordingly, their unique vulnerabilities to drugs.

Karyorelictea is a class of ciliates in the subphylum Postciliodesmatophora. Most species are members of the microbenthos community, that is, microscopic organisms found in the marine interstitial habitat, though one genus, Loxodes, is found in freshwater.

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

Myzozoa is a grouping of specific phyla within Alveolata, that either feed through myzocytosis, or were ancestrally capable of feeding through myzocytosis.

Rastrimonas is a monotypic genus of parasitic alveolates in the phylum Apicomplexa. It contains the single species Rastrimonas subtilis. It was described in 2002 from the free-living cryptomonad Chilomonas paramaecium and placed in the new genus Cryptophagus. The following year this was renamed Rastrimonas.

Vitrella brassicaformis (CCMP3155) is a unicellular alga belonging to the eukaryotic supergroup Alveolata. V. brassicaformis and its closest known relative, Chromera velia, are the only two currently described members of the phylum Chromerida, which in turn constitutes part of the taxonomically unranked group Colpodellida. Chromerida is phylogenetically closely related to the phylum Apicomplexa, which includes Plasmodium, the agent of malaria. Notably, both V. brassicaformis and C. velia are photosynthetic, each containing a complex secondary plastid. This characteristic defined the discovery of these so-called 'chromerids,' as their photosynthetic capacity positioned them to shed light upon the evolution of Apicomplexa's non-photosynthetic parasitism. Both genera lack chlorophyll b or c; these absences link the two taxonomically, as algae bearing only chlorophyll a are rare amid the biodiversity of life. Despite their similarities, V. brassicaformis differs significantly from C. velia in morphology, lifecycle, and accessory photosynthetic pigmentation. V. brassicaformis has a green color, with a complex lifecycle involving multiple pathways and a range of sizes and morphologies, while Chromera has a brown color and cycles through a simpler process from generation to generation. The color differences are due to differences in accessory pigments.

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

Parvilucifera is a genus of marine alveolates that behave as endoparasites of dinoflagellates. It was described in 1999 by biologists Fredrik Norén and Øjvind Moestrup, who identified the genus among collections of Dinophysis dinoflagellates off the coast of Sweden. Initially mistaken for products of sexual reproduction, the round bodies found within these collections were eventually recognized as sporangia, spherical structures that generate zoospores of a parasitic protist. This organism was later identified as P. infectans, the type species. The examination of this organism and its close genetic relationship to Perkinsus led to the creation of the Perkinsozoa phylum within the Alveolata group.

<span class="mw-page-title-main">Taxonomy of Protista</span> Classification of eukaryotes

A protist is any eukaryotic organism that is not an animal, plant, or fungus. The protists do not form a natural group, or clade, since they exclude certain eukaryotes with whom they share a common ancestor; but, like algae or invertebrates, the grouping is used for convenience. In some systems of biological classification, such as the popular five-kingdom scheme proposed by Robert Whittaker in 1969, the protists make up a kingdom called Protista, composed of "organisms which are unicellular or unicellular-colonial and which form no tissues". In the 21st century, the classification shifted toward a two-kingdom system of protists: Chromista and Protozoa.

Perkinsidae is a family of alveolates in the phylum Perkinsozoa, a sister group to the dinoflagellates.

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

Armophorea is a class of ciliates in the subphylum Intramacronucleata. . It was first resolved in 2004 and comprises three orders: Metopida, Clevelandellida, and Armophorida. Previously members of this class were thought to be heterotrichs because of similarities in morphology, most notably a characteristic dense arrangement of cilia surrounding their oral structures. However, the development of genetic tools and subsequent incorporation of DNA sequence information has led to major revisions in the evolutionary relationships of many protists, including ciliates. Metopids, clevelandellids, and armophorids were grouped into this class based on similarities in their small subunit rRNA sequences, making them one of two so-called "riboclasses" of ciliates, however, recent analyses suggest that Armophorida may not be related to the other two orders.

<span class="mw-page-title-main">Cortical alveolum</span> Cellular organelle found in protists

The cortical alveolum is a cellular organelle consisting of a vesicle located under the cytoplasmic membrane, to which they give support. The term "corticate" comes from an evolutionary hypothesis about the common origin of kingdoms Plantae and Chromista, because both kingdoms have cortical alveoli in at least one phylum. At least three protist lineages exhibit these structures: Telonemia, Alveolata and Glaucophyta.

<span class="mw-page-title-main">Colponemid</span> Group of predatorial flagellates

Colponemids are free-living alveolates, unicellular flagellates related to dinoflagellates, apicomplexans and ciliates. They are predators of other small eukaryotes, found in freshwater, marine and soil environments. They do not form a solid clade, but a sparse group of deep-branching alveolate lineages.

<span class="mw-page-title-main">Amoeboflagellate</span> Cellular body type

An amoeboflagellate is any eukaryotic organism capable of behaving as an amoeba and as a flagellate at some point during their life cycle. Amoeboflagellates present both pseudopodia and at least one flagellum, often simultaneously.

<span class="mw-page-title-main">Parviluciferaceae</span> Family of microscopic endoparasites

Parviluciferaceae is a family of perkinsozoans, a group of endoparasitic protists present in aquatic environments.

<span class="mw-page-title-main">Chrompodellid</span> Clade of alveolates

Chrompodellids are a clade of single-celled protists belonging to the Alveolata supergroup. It comprises two different polyphyletic groups of flagellates: the colpodellids, phagotrophic predators, and the chromerids, photosynthetic algae that live as symbionts of corals. These groups were independently discovered and described, but molecular phylogenetic analyses demonstrated that they are intermingled in a clade that is the closest relative to Apicomplexa, and they became collectively known as chrompodellids. Due to the history of their research, they are variously known in biological classification as Chromerida or Colpodellida (ICZN)/Colpodellales (ICN).

Neometanema is a genus of phagotrophic flagellates belonging to the Euglenida, a diverse group of flagellates in the phylum Euglenozoa. It is the sole genus within the monotypic family Neometanemidae and suborder Metanemina. It composes the order Natomonadida together with a closely related clade of osmotrophs known as Aphagea.

References

  1. 1 2 3 4 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.
  2. 1 2 3 4 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.
  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. 1 2 3 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: 1594. doi: 10.3389/FMICB.2017.01594 . ISSN   1664-302X. PMC   5609580 . PMID   28970818. Wikidata   Q42163896.
  5. 1 2 3 4 5 6 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. 1 2 3 4 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. 1 2 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. 1 2 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. 1 2 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. 1 2 3 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. 1 2 3 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. 1 2 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. 1 2 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. 1 2 3 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. 1 2 3 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. 1 2 3 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. 1 2 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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