Rapaza

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Rapaza
Rapaza viridis 2012 Yamaguchi et al fig1c.webp
Differential interference contrast microscopy of R. viridis capturing a Tetraselmis phytoplankton (arrowhead) with the anterior part of its cell. Scale bar: 10  μm
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Phylum: Euglenozoa
Class: Euglenida
Clade: Euglenophyceae
Order: Rapazida
Cavalier-Smith, 2016
Family: Rapazidae
Cavalier-Smith, 2016
Genus: Rapaza
Yamaguchi, Yubuki & Leander, 2012
Species:
R. viridis
Binomial name
Rapaza viridis
Yamaguchi, Yubuki & Leander, 2012 [1]

Rapaza viridis (Latin for 'green grasper') is a species of single-celled flagellate within the Euglenophyceae, a group of algae. It is the only species within the genus Rapaza, family Rapazidae and order Rapazida. It was discovered in a tide pool in British Columbia and described in 2012.

Contents

Rapaza viridis is the first known mixotroph (an organism that combines photosynthesis and ingestion of food) and kleptoplastic species within the phylum Euglenozoa. It eats microalgae by engulfing them—a process called phagocytosis—and then uses the chloroplasts from these algae to perform photosynthesis, altering the chloroplasts' structure in the process. In particular, Rapaza viridis can only feed on Tetraselmis cells native to their original environment, and will reject any other prey.

Due to its unique mode of nutrition and phylogenetic position, Rapaza viridis is considered an evolutionary step between phagotrophs and phototrophs with permanent chloroplasts. Scientists consider that the common ancestor of all Euglenophyceae (a group of algae) was similar to R. viridis. It likely stole chloroplasts from its prey—just like R. viridis—a behavior supported by the discovery of genes in Euglenophyceae that came from different types of algae through a process called horizontal gene transfer. After the divergence of R. viridis, the remaining Euglenophyceae acquired permanent plastids from Pyramimonas .

Etymology

The genus name Rapaza comes from Latin rapax 'seizing' and 'grasping', in reference to the feeding behavior of the cells. The specific name viridis, meaning 'green', references the color of the chloroplasts and algal prey cells in the process of being digested. Together, the binomial name means 'green grasper' in Latin. [1]

Taxonomy

Canada British Columbia location map 2.svg
Red pog.svg
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Type locality of Rapaza viridis [1]

The genus Rapaza was circumscribed in 2012 by protistologists Aika Yamaguchi, Naoji Yubuki and Brian S. Leander, on a study published in the journal BMC Evolutionary Biology . It was created to describe a population of euglenids isolated in 2010 from marine water samples collected at a tide pool in Pachena Beach, British Columbia, Canada. After cultivation, various growth experiments and molecular phylogenetics, the microorganisms were shown to belong to the phototrophic euglenids (Euglenophyceae) and were described as the species Rapaza viridis. The new species had a functioning chloroplast but also exhibited phagotrophy, making it the first and only example of mixotrophic euglenids. [1]

The genus was defined as including flexible mixotrophic euglenids with two unequal flagella, a minimum of one chloroplast with three membranes and pyrenoids penetrated by stacks of thylakoids, a robust stigma, a paraflagellar swelling, and a feeding pocket supported by microtubules. The species was further defined by the length and width measurements of the cells and flagella, the presence of paramylon grains in the cytoplasm, 16 pellicle strips, four rows of microtubules supporting the feeding pocket, and Tetraselmis as its preferred prey. [1]

In 2016, American protozoologist Thomas Cavalier-Smith assigned this genus to several monotypic higher-level taxa: family Rapazidae, order Rapazida and subclass Rapazia within the class Euglenophyceae, leaving the remaining euglenophyceans (Euglenales and Eutreptiales) under a new subclass Euglenophycidae. He defined these three taxa as containing phagotrophic photosynthetic eukaryote-eating (eukaryovorous) euglenids that swim in the water column instead of gliding on the substrate, and present four rows of microtubules supporting the feeding pocket instead of one as in Euglenophycidae. [2] His classification scheme was neglected by other authors in favour of treating the entirety of Euglenida (Euglenophyceae plus a variety of heterotrophic flagellates) as a class, and deprecating the use of Rapazia as a subclass. As of 2021, only Rapazidae and Rapazida are accepted taxa. [3]

Biology

Morphology

Transverse TEM image of R. viridis showing mitochondrion (M), Golgi body (G) and 16 pellicle strips (arrows). Scale bar: 1 mm Rapaza viridis 2012 Yamaguchi et al fig4a.webp
Transverse TEM image of R. viridis showing mitochondrion (M), Golgi body (G) and 16 pellicle strips (arrows). Scale bar: 1 μm

Rapaza viridis is a unicellular flagellate, a type of protist that is capable of swimming by using two flagella that differ in length and in movement. The cells are slender with a tapered posterior end, measuring approximately 10–38 μm long and 3–15 μm wide. Both flagella arise from a pocket located at the anterior end of the cell, one twice as long as the other but with the same thickness. The longer flagellum, about 1.25 times the length of the cell, is always directed forward. The shorter flagellum, about 0.65 times the cell length, is directed backward, but sometimes moves forward in an oar-like motion. Like other euglenids, cells are surrounded by a pellicle composed of 16 protein strips arranged helically below the cell membrane, and contain mitochondria with discoidal cristae. As in other spirocutes (i.e. flexible euglenids), cells of R. viridis are capable of 'metaboly' or 'euglenoid movement', which allows for active peristaltic deformation of the cell shape. Its feeding apparatus consists of one rod built of four rows of microtubules and a feeding pocket. There is a stigma composed of 1 to over 10 pigmented particles. [1] [3] The cytoplasm contains ellipsoid paramylon grains, as well as polysaccharide grains as a result of photosynthesis. [4]

Predation

Rapaza viridis 2012 Yamaguchi et al fig1e.webp
Rapaza viridis 2012 Yamaguchi et al fig1f.webp
Rapaza viridis 2012 Yamaguchi et al fig1g.webp
Rapaza viridis 2012 Yamaguchi et al fig1h.webp
LM of R. viridis cells that were starved for 7 days (left) and cells that were fed 24 hours earlier (right). Arrow: stigma, double arrowhead: chloroplast. Scale bar: 10 μm.

Rapaza viridis is an obligate mixotroph that feeds on algae through phagocytosis. [5] In the same sample where the species was discovered, the microorganism consumed native Tetraselmis algae and grew to distinctly larger and brighter cells in their presence, digesting them completely in the course of around 12 hours. When starved from the algae, cells of R. viridis became smaller and colorless, retaining at least one healthy chloroplast within its cytoplasm. During growth experiments, cells of R. viridis were exposed to a variety of different algae (e.g., Navicula , Pycnococcus , Dunaliella , Scrippsiella and non-native strains of Tetraselmis) while starved from the Tetraselmis strain that the species was found with. However, the mixotroph rejected all other preys, and could not survive for longer than 35 days without being exposed to that specific algal strain. Even under constant supply of that strain, the species could not survive for more than a week in the absence of a light source for photosynthesis. [1]

Upon exposition to the native Tetraselmis strain, R. viridis cells enter a feeding frenzy: they capture algae with the anterior part of the cell and drag the prey, either swimming backward in a spiral pattern or rotating rapidly. The euglenid can gradually peel away the theca (cell covering) of Tetraselmis through repeated peristaltic euglenoid movement (or metaboly), and then engulf the naked prey cell, or engulf the cell with an intact theca and afterwards discharge the theca. The entire process takes between 5 and 40 minutes, but a single R. viridis individual can contain several ingested Tetraselmis cells. [1]

Chloroplasts and kleptoplasty

When describing Rapaza viridis, two types of distinct chloroplasts were reported: one belonging to the ingested green alga Tetraselmis, and one homologous to the chloroplasts seen in phototrophic euglenids. The former were surrounded by two membranes and contained an eyespot and pyrenoids surrounded by starch, without any penetrating thylakoids. The latter were surrounded by three membranes and contained 1–3 pyrenoids, as well as thylakoids in stacks of three that penetrate the pyrenoids. [1] From these observations, it was inferred that R. viridis possesses 'canonical' plastids, i.e. completely functional plastids equivalent to those seen in other Euglenophyceae, which depend on the host cell for survival and multiply and evolve with it. [4]

However, subsequent studies revealed that R. viridis does not have canonical plastids. Instead, it extracts and temporarily retains the chloroplasts of its prey for its own use, a process known as kleptoplasty ('stealing of plastids'). After phagocytosis of the algal prey, its cell membrane is digested [6] and the plastids are separated from the other cellular components, which are later excreted from the host cell. Then, the stolen plastids ('kleptoplasts') are transformed until they resemble canonical plastids: they are divided into smaller fragments by fission, the green algal pyrenoid surrounded by starch disappears, smaller pyrenoids penetrated by thylakoids are formed, the starch grains gradually disappear, and a three-membrane envelope is displayed (two membranes from the original chloroplast and one membrane belonging to the food vacuole). [4]

Rapaza viridis needs a regular influx of kleptoplasts, obtained through the phagocytosis of its prey. Without acquiring new kleptoplasts, the cells cannot survive for more than 35 days. During starvation, the remaining kleptoplasts are gradually degraded, and vacuoles are formed to recycle intracellular substances. [4]

Distribution and habitat

The species Rapaza viridis was reported in a tide pool in Pachena Beach, British Columbia. Because of this location, it is considered a marine species. [1] In addition, the TARA Oceans expedition and Ocean Sampling Day campaign recovered an enormous diversity of environmental sequences that belong to or are most closely related to Rapaza, particularly within the Mediterranean Sea. These sequences, named Rapaza-like operational taxonomic unit (OTUs), were more abundant in waters with high temperatures (20–30°C). [7]

Evolution

According to phylogenetic analyses, Rapaza viridis is the sister group to all other Euglenophyceae. [8] This phylogenetic position is consistent with its place as an evolutionary step between the completely phagotrophic peranemids and the phototrophic Euglenophyceae, because mixotrophy is considered the transitional state during the establishment of the endosymbiotic prey cell and the phagotrophic host cell. It is also consistent with other intermediate characters. For example, it is the only eukaryote-eating euglenid that, instead of gliding on the substrate, is capable of swimming in the water column, a pattern only seen in phototrophs. [1] It is also the only euglenophycean that only presents the MAT paralogue of the enzyme methionine adenosyltransferase, found in heterotrophic euglenids, whereas the remaining euglenophyceans acquired the MATX paralogue after the split from Rapaza. [9]

Spirocuta
Euglenophyceae
chloroplasts,
MATX paralogue

Rapaza

kleptoplasty,
HGT from algae

Peranemida

Anisonemia

"Ploeotiida"

Petalomonadida

Phylogenetic position of Rapaza within the Euglenida, [10] with sublabels indicating evolutionary steps towards permanent chloroplasts. [4]

Rapaza viridis is the first case of kleptoplasty within Euglenozoa. Particularly, its chloroplasts are obtained from the green alga Tetraselmis . Transcriptomic and genomic analyses revealed that there are genes encoded in the nucleus of R. viridis and other Euglenophyceae for plastid-targeted proteins acquired from chloroplasts of many different algae (including algae from the "red lineage", i.e. red and chromalveolate algae) through multiple ancient events of horizontal gene transfer. Due to these discoveries, the leading hypothesis is that the last common ancestor of all Euglenophyceae was not a phototroph, but an alga-eating phagotroph without permanent plastids that could have exhibited kleptoplasty, much like Rapaza viridis. This common ancestor horizontally acquired the protein targeting system from many algae after prolonged coexistence (from both kleptoplasty and predation). This targeting system could have been involved in the establishment of permanent plastids in the remaining Euglenophyceae, which originated from the green alga Pyramimonas . Additionally, Tetraselmis-derived genes are abundant in other Euglenophyceae, while Pyramimonas-derived genes are minor in Rapaza, meaning that the close association with Pyramimonas began after the divergence of Rapaza. [4]

In addition to kleptoplast-targeted proteins, Rapaza viridis obtained a nucleus-coded nitrate reductase through horizontal gene transfer from ancient algal prey. Nitrate reductases are a key component of phototrophic organisms, since it allows for the assimilation of inorganic nitrogen, which heterotrophic organisms are not capable of. This enzyme, known as RvNaRL, is a crucial step of metabolic integration in the early stages of secondary endosymbiosis towards permanent phototrophy. [11] [12]

Related Research Articles

<span class="mw-page-title-main">Chloroplast</span> Plant organelle that conducts photosynthesis

A chloroplast is a type of membrane-bound organelle known as a plastid that conducts photosynthesis mostly in plant and algal cells. The photosynthetic pigment chlorophyll captures the energy from sunlight, converts it, and stores it in the energy-storage molecules ATP and NADPH while freeing oxygen from water in the cells. The ATP and NADPH is then used to make organic molecules from carbon dioxide in a process known as the Calvin cycle. Chloroplasts carry out a number of other functions, including fatty acid synthesis, amino acid synthesis, and the immune response in plants. The number of chloroplasts per cell varies from one, in unicellular algae, up to 100 in plants like Arabidopsis and wheat.

<span class="mw-page-title-main">Euglenozoa</span> Phylum of protozoans

Euglenozoa are a large group of flagellate Discoba. They include a variety of common free-living species, as well as a few important parasites, some of which infect humans. Euglenozoa are represented by four major groups, i.e., Kinetoplastea, Diplonemea, Euglenida, and Symbiontida. Euglenozoa are unicellular, mostly around 15–40 μm (0.00059–0.00157 in) in size, although some euglenids get up to 500 μm (0.020 in) long.

<span class="mw-page-title-main">Euglenid</span> Class of protozoans

Euglenids or euglenoids are one of the best-known groups of flagellates. They are excavate eukaryotes of the phylum Euglenophyta, classified as class Euglenida or Euglenoidea. Euglenids are commonly found in freshwater, especially when it is rich in organic materials, with a few marine and endosymbiotic members. Many euglenids feed by phagocytosis, or strictly by diffusion. A monophyletic group known as Euglenophyceae have chloroplasts and produce their own food through photosynthesis. This group is known to contain the carbohydrate paramylon.

<span class="mw-page-title-main">Kleptoplasty</span> Form of algae symbiosis

Kleptoplasty or kleptoplastidy is a process in symbiotic relationships whereby plastids, notably chloroplasts from algae, are sequestered by the host. The word is derived from Kleptes (κλέπτης) which is Greek for thief. The alga is eaten normally and partially digested, leaving the plastid intact. The plastids are maintained within the host, temporarily continuing photosynthesis and benefiting the host.

<span class="mw-page-title-main">Euglenophyceae</span> Unicellular algae

Euglenophyceae (ICBN) or Euglenea (ICZN) is a group of single-celled algae belonging to the phylum Euglenozoa. They have chloroplasts originated from an event of secondary endosymbiosis with a green alga. They are distinguished from other algae by the presence of paramylon as a storage product and three membranes surrounding each chloroplast.

<i>Pyramimonas</i> Genus of algae

Pyramimonas is a genus of green algae in the order Pyramimonadales. Phototropic euglenids inherited their plastids from a close relative of Pyramimonas which was an endosymbiont inside phagotrophic eukaryovorous euglenids.

<span class="mw-page-title-main">Euglenales</span> Order of flagellate eukaryotes

Euglenales is an order of flagellates in the phylum Euglenozoa. The family includes the most well-known euglenoid genus, Euglena, as well as other common genera like Phacus and Lepocinclis.

<span class="mw-page-title-main">Euglenaceae</span> Family of flagellate eukaryotes

Euglenaceae is a family of flagellates in the phylum Euglenozoa. The family includes the most well-known euglenoid genus, Euglena.

<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.

<i>Calkinsia</i> Genus of algae

Calkinsia is a monotypic genus of excavates comprising the single species Calkinsia aureus. It lives in low-oxygen seafloor environments. It is not classified in any of the three well-known groups of the Euglenozoa, but is placed in its own group, the Symbiontida. Some authors have classified Calkinsia alongside Postgaardi, but Postgaardi has not been studied well enough to test this hypothesis.

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

Rhodomonas is a genus of cryptomonads. It is characterized by its red colour, the square-shaped plates of its inner periplast, its short furrow ending in a gullet, and a distinctly shaped chloroplast closely associated with its nucleomorph. Historically, Rhodomonas was characterized by its red chloroplast alone, but this no longer occurs as its taxonomy has become increasingly based on molecular and cellular data. Currently, there is some debate about the taxonomic validity of Rhodomonas as a genus and further research is needed to verify its taxonomic status. Rhodomonas is typically found in marine environments, although freshwater reports exist. It is commonly used as a live feed for various aquaculture species.

<i>Vaucheria litorea</i> Species of alga

Vaucheria litorea is a species of yellow-green algae (Xanthophyceae). It grows in a filamentous fashion. V. litorea is a common intertidal species of coastal brackish waters and salt marshes of the Northern Atlantic, along the coasts of Europe, North America and New Zealand. It is also found in the Eastern Pacific coasts of Washington state. It is found to be able to tolerate a large range of salinities, making it euryhaline.

Heteronema is a genus of phagotrophic, flagellated euglenoids that are most widely distributed in fresh water environments. This genus consists of two very distinguishable morphogroups that are phylogenetically closely related. These morphogroups are deciphered based on shape, locomotion and other ultrastructural traits. However, this genus does impose taxonomic problems due to the varying historical descriptions of Heteronema species and its similarity to the genus Paranema. The species H. exaratum, was the first heteronemid with a skidding motion to be sequenced, which led to the discovery that it was not closely related to H. scaphrum, contrary to what was previously assumed, but instead to a sister group of primary osmotrophs. This suggests that skidding heteronemids can also be distinguished phylogenetically, being more closely related to Anisoma, Dinema and Aphageae, than to other species within Heteronema.

<i>Urceolus</i> Genus of flagellates

Urceolus is a genus of heterotrophic flagellates belonging to the Euglenozoa, a phylum of single-celled eukaryotes or protists. Described by Russian biologist Konstantin Mereschkowsky in 1877, its type species is Urceolus alenizini. Species of this genus are characterized by deformable flask-shaped cells that exhibit at least one flagellum that is active at the tip, arising from a neck-like structure that also hosts the feeding apparatus. They are found in a variety of water body sediments across the globe. According to evolutionary studies, Urceolus belongs to a group of Euglenozoa known as peranemids, closely related to the euglenophyte algae.

<i>Ploeotia</i> Genus of flagellates

Ploeotia is a genus of heterotrophic flagellates belonging to the Euglenida, a diverse group of flagellated protists in the phylum Euglenozoa. Species of Ploeotia are composed of rigid cells exhibiting two flagella. The genus was described by Félix Dujardin in 1841.

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

The peranemids are a group of phagotrophic flagellates, single-celled eukaryotes or protists. They belong to the Euglenida, a diverse lineage of flagellates that contains the closely related euglenophyte algae. Like these algae, peranemids have flexible cells capable of deformation or metaboly, and have one or two flagella in the anterior region of the cell. They are classified as family Peranemidae (ICZN) or Peranemataceae (ICBN) within the monotypic order Peranemida (ICZN) or Peranematales (ICBN).

<span class="mw-page-title-main">Spirocuta</span> Group of flagellates with flexible cells

Spirocuta is a clade of euglenids, single-celled eukaryotes or protists belonging to the phylum Euglenozoa. They are distinguished from other euglenids by active deformation of their cell shape, a process called euglenid motion or metaboly. This is made possible by a high number of spirally arranged protein strips that run below their cell membrane and confer the cell with flexibility. These strips compose the helicoidal pellicle, a trait referenced by the alternative name Helicales.

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

Anisonemia is a clade of single-celled protists belonging to the phylum Euglenozoa, relatives of the Euglenophyceae algae. They are flagellates, with two flagella for locomotion. Anisonemia includes various phagotrophic species and a group of primary osmotrophic protists known as Aphagea.

Eutreptiaceae (ICN) or Eutreptiidae (ICZN) is a family of algae in the class Euglenophyceae. It is the only family within the monotypic order Eutreptiales (ICN) or Eutreptiida (ICZN). It contains predominantly marine single-celled flagellates with photosynthetic chloroplasts.

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 5 6 7 8 9 10 11 Aika Yamaguchi; Naoji Yubuki; Brian S Leander (8 March 2012). "Morphostasis in a novel eukaryote illuminates the evolutionary transition from phagotrophy to phototrophy: description of Rapaza viridis n. gen. et sp. (Euglenozoa, Euglenida)". BMC Ecology and Evolution . 12 (1): 29. doi:10.1186/1471-2148-12-29. ISSN   1471-2148. PMC   3374381 . PMID   22401606. Wikidata   Q28728551.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  2. ↑ Thomas Cavalier-Smith (15 September 2016). "Higher classification and phylogeny of Euglenozoa". European Journal of Protistology . 56: 250–276. doi:10.1016/J.EJOP.2016.09.003. ISSN   0932-4739. PMID   27889663. Wikidata   Q39151632.
  3. 1 2 Alexei Y. Kostygov; Anna Karnkowska; Jan Votýpka; Daria Tashyreva; Kacper Maciszewski; Vyacheslav Yurchenko; Julius Lukeš (10 March 2021). "Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses". Open Biology . 11: 200407. doi:10.1098/RSOB.200407. ISSN   2046-2441. PMC   8061765 . PMID   33715388. Wikidata   Q125548575.
  4. 1 2 3 4 5 6 Anna Karnkowska; Naoji Yubuki; Moe Maruyama; et al. (16 March 2023). "Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis". Proceedings of the National Academy of Sciences of the United States of America . 120 (12): e2220100120. doi:10.1073/PNAS.2220100120. ISSN   0027-8424. PMC   10041101 . PMID   36927158. Wikidata   Q125824653.
  5. ↑ 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.
  6. ↑ Andrzej Bodył (5 October 2017). "How to Lose the Plasmalemma? Lessons From Ciliates, Dinoflagellates and Euglenids". BioEssays . 39 (11). doi:10.1002/BIES.201700149. ISSN   0265-9247. PMID   28980324. Wikidata   Q49587603.
  7. ↑ Soňa Lukešová; Michał Karlicki; Lucia Tomečková Hadariová; Jana Szabová; Anna Ewa Karnkowska; Vladimír Hampl (26 December 2019). "Analyses of environmental sequences and two regions of chloroplast genomes revealed the presence of new clades of photosynthetic euglenids in marine environments". Environmental Microbiology Reports. 12 (1): 78–91. doi:10.1111/1758-2229.12817. ISSN   1758-2229. PMID   31845515. Wikidata   Q92036403.
  8. ↑ Antonia S. Rackevei; Anna Karnkowska; Matthias Wolf (7 December 2022). "18S rDNA sequence-structure phylogeny of the Euglenophyceae (Euglenozoa, Euglenida)". Journal of Eukaryotic Microbiology . 70 (2): e12959. doi:10.1111/JEU.12959. ISSN   1066-5234. PMID   36478494. Wikidata   Q125859535.
  9. ↑ Jana Szabová; Naoji Yubuki; Brian S Leander; Richard E Triemer; Vladimír Hampl (11 February 2014). "The evolution of paralogous enzymes MAT and MATX within the Euglenida and beyond". BMC Ecology and Evolution . 14: 25. doi:10.1186/1471-2148-14-25. ISSN   1471-2148. PMC   3923989 . PMID   24517416. Wikidata   Q35092071.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  10. ↑ Gordon Lax; Alastair G. B. Simpson (16 August 2020). "The Molecular Diversity of Phagotrophic Euglenids Examined Using Single-cell Methods". Protist . 171 (5): 125757. doi:10.1016/J.PROTIS.2020.125757. ISSN   1434-4610. PMID   33126020. Wikidata   Q101127864.
  11. ↑ Moe Maruyama; Tsuyoshi Kagamoto; Yuga Matsumoto; Ryo Onuma; Shin-ya Miyagishima; Goro Tanifuji; Masami Nakazawa; Yuichiro Kashiyama (22 May 2023). "Horizontally Acquired Nitrate Reductase Realized Kleptoplastic Photoautotrophy of Rapaza viridis". Plant and Cell Physiology. 64 (9): 1082–1090. doi:10.1093/PCP/PCAD044. ISSN   0032-0781. PMID   37217185. Wikidata   Q125859288.
  12. ↑ Yoshinori Tsuji (3 July 2023). "Kleptoplasty Relies on a Host-Derived Component in the Euglenid Protist, Rapaza viridis". Plant and Cell Physiology. 64 (9): 1079–1081. doi:10.1093/PCP/PCAD070. ISSN   0032-0781. PMID   37464867. Wikidata   Q125859336.
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