Chrompodellid

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Chrompodellids
Vitrella brassicaformis LM Michalek 2020.png
Typical life cycle stages of Vitrella brassicaformis , a chromerid (vc: vegetative cell, zs: zoosporangium, as: autosporangium)
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Myzozoa
Class: Chromeridophyceae
Molinari & Guiry 2023 [1]
Subclass: Chromeridophycidae
Mylnikov et al. 2000 [2]
Order: Colpodellales
Cavalier-Smith 1993 [3] emend. Adl et al. 2005, 2019 [4] [1]
Type genus
Colpodella
Cienkowsky 1865 [3]
Families [4] [1]
Synonyms
  • Apicomonadea Cavalier-Smith 1993 emend. 2017 [5]
  • Chromerida Moore et al. 2008 [6]
  • Chromeridophyta Guiry 2024 [7]

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).

Description and life cycle

Chrompodellids are a clade of unicellular protists containing two functionally different groups: the photosynthetic "chromerids" and the predatory phagotrophic "colpodellids". Like other Alveolata, they present tubular mitochondrial cristae and highly flattened cortical alveoli [8] with microtubules underneath. They exhibit a conoid-like structure similar to that of apicomplexans, with an apical complex, a micropore and a rostrum. They live as flagellates with two anisokont (i.e. differently sized) flagella [3] that are heterodynamic (i.e. move in different patterns). [9] Some species exhibit thin mastigonemes in their anterior flagellum, while others bear bulbs. [9] Some species are capable of forming cysts. [4]

Colpodellids

Colpodellids, represented by the genera Colpodella , Alphamonas , Voromonas and Chilovora , are free-living predatory phagotrophic flagellates. [9] They live as biflagellated single cells, 5–20 μm in length, with an open conoid and rhoptries used to hunt. They present genetic sequences of non-photosynthetic plastids, an evidence of their phototroph ancestry. [8]

Some species, considered ectoparasites, do not ingest prey cells, but rather fully or partially "suck" their contents, a process known as myzocytosis, common among alveolates. [9] [10] They feed on bacteria and other protozoa, such as bodonids, chrysomonads, bicosoecids, percolomonads and ciliates. [11] After feeding, they internalize their flagella, become cysts and divide into tetrads, similarly to the development of zoospores in Chromera . The cells conjugate after leaving the cyst, which could imply a sexual stage. [8]

Chromerids

Chromerids, represented by the genera Chromera and Vitrella , are photosynthetic protists, and are thus considered algae. They exist in association with corals. For most of their life cycle, they live as round (coccoid) brownish immobile vegetative cells called autospores, surrounded by a thick resistant cell wall. They contain one chloroplast in each cell, [8] with chlorophyll a as their only chlorophyll, [12] violaxanthin, and β-carotene. [8]

The two genera are markedly different from each other, both in phylogeny and life cycles. Chromera autospores are 5–7 μm in diameter. They asexually reproduce through binary division to develop autosporangia, which in turn harbor 2–4 autospores under an additional membrane. They also form zoosporangia, up to 15 μm in diameter, capable of generating 2–10 flagellated zoospores that strongly resemble colpodellids. This dispersal process is similar to the schizogony of apicomplexans. Sexual reproduction has not been observed. Under adverse environmental conditions, they form resistant cysts that remain viable for years. Similarly to apicomplexans, they undergo closed mitosis, without dissolving the nuclear envelope. [8] In addition, Chromera produces high amounts of an exclusive type of isofucoxanthin. [6]

Vitrella autospores, by contrast, start measuring 3 μm and grow up to 40 μm before transforming into sporangia that generate dozens of autospores or zoospores. There are two types of Vitrella zoospores: one is generated by budding from the mother cell and exhibits flagella outside the cytoplasm, the other develops axonemes and flagella within their cytoplasm and are ejected from the mother cell after maturing, though both types lack a pseudo-conoid. Some zoospores fuse, possibly representing a sexual stage in the life cycle. [8] In addition, Vitrella produces vaucheriaxanthin. [13]

Evolution

Chrompodellids are the closest living relatives of the apicomplexan parasites, which evolved from a photosynthetic myzozoan ancestor, making chromerids the last remaining photosynthetic members of an otherwise parasitic clade within Alveolata. [14] The apicomplexans, chrompodellids, perkinsids and dinoflagellates constitute the clade Myzozoa, characterized by the apical complex and plastids derived from an event of secondary endosymbiosis with a red alga. The photosynthetic ability of these plastids was eventually lost in apicomplexans, colpodellids, perkinsids and other groups that transitioned into a predatory or parasitic lifestyle. [8] The following cladogram summarizes alveolate relationships and the internal relationships among most genera within the chrompodellid clade (chromerids marked with asterisks): [15] [12] [16]

Alveolata

Systematics

Taxonomic history

In 1993, protozoologist Thomas Cavalier-Smith described the order Colpodellida (under the ICZN, later regularized as Colpodellales in accordance to the ICN) [1] to contain what he considered one of the "most primitive flagellate apicomplexans", the genus Colpodella . This order was introduced in the class Apicomonadea along with the Perkinsida. [3] Cavalier-Smith treats this class as a member of the phylum Apicomplexa, while "true" apicomplexans are united under the name Sporozoa. [5] Although the inclusion of colpodellids within apicomplexans was not supported by other authors, phylogenetic studies demonstrated that they were sister clades. [17]

The first chromerid alga, Chromera velia , was discovered and isolated from Australian corals in 2001. It was described in 2008 as the first member of a new phylum Chromerida, followed by Vitrella brassicaformis in 2012. [13] They showed morphological resemblance to colpodellids and other myzozoans. [12] In the following years, phylogenetic studies reported the evolutionary proximity between colpodellids and chromerid algae. [6] This was supported by the discovery of retained vestigial plastids in some colpodellid species. [18] In 2015 there was strong support for a clade containing the two groups, phylogenetically mixed with each other, which rendered both as polyphyletic. The clade was given the provisional name "chrompodellids", [15] later referred to as Chrompodellida by posterior studies. [19]

Between 2004 and 2017, Cavalier-Smith retained the classification scheme of Apicomonadea, from which he excluded Perkinsida, leaving only colpodellids and chromerids across multiple orders. In addition, several genera of flagellates were added on the basis of morphological data: Algovora, Microvorax and Dinomonas. [20] Due to lacking molecular data, these genera have been excluded from later classifications. [4] Two genera, Chilovora and Alphamonas , were eventually rejected in his classification, [5] but later revisions by other authors maintain them as independent genera supported by molecular data. [4]

The treatment of chrompodellids as a subgroup of Apicomplexa, under the name of Apicomonadea, was rejected by the International Society of Protistologists. In a 2019 revision of eukaryotic classification, protistologists emended the previous name Colpodellida to contain all chrompodellids, and treated it as a direct subgroup of Alveolata, independent from Apicomplexa. [4] Later, phycologists advocated for this treatment as a separate phylum, and regularized it under the name of Chromerida or Chromeridophyta, composed of a single class Chromeridophyceae and a single order Colpodellales, in accordance to the nomenclatural rules of the ICN. [1] [7] However, other authors consider them a subgroup of the phylum Myzozoa, together with apicomplexans, perkinsozoans and dinoflagellates. [15] [5] [8]

Classification

As of 2023, chrompodellids are divided into four families and seven genera: [4] [1]

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.

<span class="mw-page-title-main">Chromista</span> Eukaryotic biological kingdom

Chromista is a proposed but polyphyletic biological kingdom, refined from the Chromalveolata, consisting of single-celled and multicellular eukaryotic species that share similar features in their photosynthetic organelles (plastids). It includes all eukaryotes whose plastids contain chlorophyll c and are surrounded by four membranes. If the ancestor already possessed chloroplasts derived by endosymbiosis from red algae, all non-photosynthetic Chromista have secondarily lost the ability to photosynthesise. Its members might have arisen independently as separate evolutionary groups from the last eukaryotic common ancestor.

<span class="mw-page-title-main">Labyrinthulomycetes</span> Class of protists that produce a filamentous network

Labyrinthulomycetes (ICBN) or Labyrinthulea (ICZN) is a class of protists that produce a network of filaments or tubes, which serve as tracks for the cells to glide along and absorb nutrients for them. The two main groups are the labyrinthulids and thraustochytrids. They are mostly marine, commonly found as parasites on algae and seagrasses or as decomposers on dead plant material. They also include some parasites of marine invertebrates and mixotrophic species that live in a symbiotic relationship with zoochlorella.

<span class="mw-page-title-main">Chromalveolata</span> Group of eukaryotic organisms

Chromalveolata was a eukaryote supergroup present in a major classification of 2005, then regarded as one of the six major groups within the eukaryotes. It was a refinement of the kingdom Chromista, first proposed by Thomas Cavalier-Smith in 1981. Chromalveolata was proposed to represent the organisms descended from a single secondary endosymbiosis involving a red alga and a bikont. The plastids in these organisms are those that contain chlorophyll c.

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

Telonemia is a phylum of microscopic eukaryotes commonly known as telonemids. They are unicellular free-living flagellates with a unique combination of cell structures, including a highly complex cytoskeleton unseen in other eukaryotes.

<span class="mw-page-title-main">Ochrophyte</span> Phylum of algae

Ochrophytes, also known as heterokontophytes or stramenochromes, are a group of algae. They are the photosynthetic stramenopiles, a group of eukaryotes, organisms with a cell nucleus, characterized by the presence of two unequal flagella, one of which has tripartite hairs called mastigonemes. In particular, they are characterized by photosynthetic organelles or plastids enclosed by four membranes, with membrane-bound compartments called thylakoids organized in piles of three, chlorophyll a and c as their photosynthetic pigments, and additional pigments such as β-carotene and xanthophylls. Ochrophytes are one of the most diverse lineages of eukaryotes, containing ecologically important algae such as brown algae and diatoms. They are classified either as phylum Ochrophyta or Heterokontophyta, or as subphylum Ochrophytina within phylum Gyrista. Their plastids are of red algal origin.

<span class="mw-page-title-main">Phylum</span> High level taxonomic rank for organisms sharing a similar body plan

In biology, a phylum is a level of classification or taxonomic rank below kingdom and above class. Traditionally, in botany the term division has been used instead of phylum, although the International Code of Nomenclature for algae, fungi, and plants accepts the terms as equivalent. Depending on definitions, the animal kingdom Animalia contains about 31 phyla, the plant kingdom Plantae contains about 14 phyla, and the fungus kingdom Fungi contains about 8 phyla. Current research in phylogenetics is uncovering the relationships among phyla within larger clades like Ecdysozoa and Embryophyta.

<span class="mw-page-title-main">SAR supergroup</span> Eukaryotes superphylum

SAR or Harosa is a highly diverse clade of eukaryotes, often considered a supergroup, that includes stramenopiles (heterokonts), alveolates, and rhizarians. It is a node-based taxon, including all descendants of the three groups' last common ancestor, and comprises most of the now-rejected Chromalveolata. Their sister group has been found to be telonemids, with which they make up the TSAR clade.

<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.

<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.

<span class="mw-page-title-main">Perkinsea</span> Group of intracellular parasites

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.

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">Haptista</span> Group of protists

Haptista is a proposed group of protists made up of centrohelids and haptophytes. Phylogenomic studies indicate that Haptista, together with Ancoracysta twista, forms a sister clade to the SAR+Telonemia supergroup, but it may also be sister to the Cryptista (+Archaeplastida). It is thus one of the earliest diverging Diaphoretickes.

Rhodelphis is a single-celled archaeplastid that lives in aquatic environments and is the sister group to red algae and possibly Picozoa. While red algae have no flagellated stages and are generally photoautotrophic, Rhodelphis is a flagellated predator containing a non-photosynthetic plastid. This group is important to the understanding of plastid evolution because they provide insight into the morphology and biochemistry of early archaeplastids. Rhodelphis contains a remnant plastid that is not capable of photosynthesis, but may play a role in biochemical pathways in the cell like heme synthesis and iron-sulfur clustering. The plastid does not have a genome, but genes are targeted to it from the nucleus. Rhodelphis is ovoid with a tapered anterior end bearing two perpendicularly-oriented flagella.

<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">Parviluciferaceae</span> Family of microscopic endoparasites

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

References

  1. 1 2 3 4 5 6 Eduardo A. Molinari-Novoa; Michael D. Guiry (30 October 2023). "Nomenclatural notes on algae. VIII. Automatically typified names for some groups of alveolates" (PDF). Notulae Algarum. 2023 (304): 1–3.
  2. ↑ A.P. Mylnikov; M.V. Krylov; A.O. Frolov (2000). "Таксономический ранг и место в системе протистов Colpodellida" Taksonomicheskiy rang i mesto v sisteme protistov Colpodellida [Taxonomic rank and place of Colpodellida in a system](PDF). Parazitologiya (in Russian). 34 (1): 3–15.
  3. 1 2 3 4 T Cavalier-Smith (December 1993). "Kingdom protozoa and its 18 phyla". Microbiological Reviews. 57 (4): 953–94. ISSN   0146-0749. PMC   372943 . PMID   8302218. Wikidata   Q24634634.
  4. 1 2 3 4 5 6 7 8 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.
  5. 1 2 3 4 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.
  6. 1 2 3 4 Moore RB; Oborník M; Janouskovec J; Chrudimský T; Vancová M; Green DH; Wright SW; Davies NW; et al. (February 2008). "A photosynthetic alveolate closely related to apicomplexan parasites". Nature. 451 (7181): 959–963. Bibcode:2008Natur.451..959M. doi:10.1038/nature06635. PMID   18288187. S2CID   28005870.
  7. 1 2 Michael D. Guiry (21 January 2024). "How many species of algae are there? A reprise. Four kingdoms, 14 phyla, 63 classes and still growing". Journal of Phycology . 00: 1–15. doi:10.1111/JPY.13431. ISSN   0022-3646. PMID   38245909. Wikidata   Q124684077.
  8. 1 2 3 4 5 6 7 8 9 Zoltán Füssy; Miroslav Oborník (2017). "Chromerids and Their Plastids". Advances in Botanical Research. 84: 187–218. doi:10.1016/BS.ABR.2017.07.001. ISSN   0065-2296. Wikidata   Q57761541.
  9. 1 2 3 4 A. P. Mylnikov (1 November 2009). "Ultrastructure and Phylogeny of Colpodellids (Colpodellida, Alveolata)". Russian Academy of Sciences. Biology Bulletin (6): 685–694. ISSN   1062-3590. PMID   20143628. Wikidata   Q82839650.
  10. ↑ Z. M. Myl'nikova; A. P. Myl'nikov (20 September 2009). "The morphology of predatory flagellate Colpodella pseudoedax Mylnikov et Mylnikov, 2007 (Colpodellida, Alveolata)". Inland Water Biology. 2 (3): 199–204. doi:10.1134/S199508290903002X. ISSN   1995-0829. Wikidata   Q124751768.
  11. ↑ A. P. Mylnikov; Z. M. Mylnikova (24 September 2008). "Feeding spectra and pseudoconoid structure in predatory alveolate flagellates". Inland Water Biology. 1 (3): 210–216. doi:10.1134/S1995082908030036. ISSN   1995-0829. Wikidata   Q124744550.
  12. 1 2 3 Jan Michálek (2020). Genomes of Chromerid Algae (PDF) (PhD thesis). Czech Republic: University of South Bohemia in České Budějovice.
  13. 1 2 3 Oborník, M; Modrý, D; Lukeš, M; Cernotíková-Stříbrná, E; Cihlář, J; Tesařová, M; Kotabová, E; Vancová, M; Prášil, O; Lukeš, J (2012). "Morphology, Ultrastructure and Life Cycle of Vitrella brassicaformis n. sp., n. gen., a Novel Chromerid from the Great Barrier Reef". Protist. 163 (2): 306–323. doi:10.1016/j.protis.2011.09.001. PMID   22055836.
  14. ↑ Woo, Y. H.; Ansari, H.; Otto, T. D.; Klinger, C. M.; Kolisko, M.; Michálek, J.; Saxena, A.; Shanmugam, D.; Tayyrov, A.; Veluchamy, A.; Ali, S.; Bernal, A.; Del Campo, J.; Cihlář, J.; Flegontov, P.; Gornik, S. G.; Hajdušková, E.; Horák, A.; Janouškovec, J.; Katris, N. J.; Mast, F. D.; Miranda-Saavedra, D.; Mourier, T.; Naeem, R.; Nair, M.; Panigrahi, A. K.; Rawlings, N. D.; Padron-Regalado, E.; Ramaprasad, A.; et al. (2015). "Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites". eLife. 4: e06974. doi: 10.7554/eLife.06974 . PMC   4501334 . PMID   26175406.
  15. 1 2 3 Jan Janouškovec; Denis Tikhonenkov; Fabien Burki; Alexis T Howe; Martin Kolísko; Alexander P Mylnikov; Patrick John Keeling (25 February 2015). "Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives". Proceedings of the National Academy of Sciences of the United States of America . 112 (33): 10200–10207. Bibcode:2015PNAS..11210200J. doi:10.1073/PNAS.1423790112. ISSN   0027-8424. PMC   4547307 . PMID   25717057. Wikidata   Q30662251.
  16. 1 2 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.
  17. ↑ Olga N Kuvardina; Brian S Leander; Vladimir V Aleshin; Alexander P Myl'nikov; Patrick John Keeling; Timur G Simdyanov (1 November 2002). "The phylogeny of colpodellids (Alveolata) using small subunit rRNA gene sequences suggests they are the free-living sister group to apicomplexans". Journal of Eukaryotic Microbiology . 49 (6): 498–504. doi:10.1111/J.1550-7408.2002.TB00235.X. ISSN   1066-5234. PMID   12503687. Wikidata   Q34167276.
  18. ↑ Gillian H Gile; Claudio H Slamovits (2014). "Transcriptomic analysis reveals evidence for a cryptic plastid in the colpodellid Voromonas pontica, a close relative of chromerids and apicomplexan parasites". PLOS One . 9 (5): e96258. Bibcode:2014PLoSO...996258G. doi:10.1371/JOURNAL.PONE.0096258. ISSN   1932-6203. PMC   4010437 . PMID   24797661. Wikidata   Q28657955.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  19. ↑ Andrea Valigurová; Isabelle Florent (2 July 2021). "Nutrient Acquisition and Attachment Strategies in Basal Lineages: A Tough Nut to Crack in the Evolutionary Puzzle of Apicomplexa". Microorganisms. 9 (7): 1430. doi: 10.3390/microorganisms9071430 . PMC   8303630 . PMID   34361866.
  20. 1 2 3 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.
  21. ↑ Miroslav Oborník; Marie Vancová; De-Hua Lai; Jan Janouškovec; Patrick John Keeling; Julius Lukeš (1 January 2011). "Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of apicomplexa, Chromera velia". Protist . 162 (1): 115–130. doi:10.1016/J.PROTIS.2010.02.004. ISSN   1434-4610. PMID   20643580. Wikidata   Q34126892.
  22. ↑ L. Cienkowski (1865). "Beiträge zur Kenntniss der Monaden" (PDF). Archiv für Mikroskopische Anatomie. 1 (1): 203–232. doi:10.1007/BF02961414. S2CID   84323025.
  23. ↑ Ruth Patten (October 1936). "Notes on a New Protozoon, Piridium sociabile n.gen., n.sp., from the Foot of Buccinum undatum". Parasitology . 28 (04): 502. doi:10.1017/S003118200002268X. ISSN   0031-1820. Wikidata   Q54495349.
  24. ↑ Jan Janouškovec; Gita Paskerova; Tatiana S Miroliubova; Kirill V Mikhailov; Thomas Birley; Vladimir V. Aleoshin; Timur Simdyanov (16 August 2019). "Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles". eLife . 8. doi:10.7554/ELIFE.49662. ISSN   2050-084X. PMC   6733595 . PMID   31418692. Wikidata   Q83229299.{{cite journal}}: CS1 maint: unflagged free DOI (link)
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