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).

Contents

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, 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, [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">Flagellate</span> Group of protists with at least one whip-like appendage

A flagellate is a cell or organism with one or more whip-like appendages called flagella. The word flagellate also describes a particular construction characteristic of many prokaryotes and eukaryotes and their means of motion. The term presently does not imply any specific relationship or classification of the organisms that possess flagella. However, several derivations of the term "flagellate" are more formally characterized.

<span class="mw-page-title-main">Stramenopile</span> Clade of eukaryotes

The Stramenopiles, also called Heterokonts, are a clade of organisms distinguished by the presence of stiff tripartite external hairs. In most species, the hairs are attached to flagella, in some they are attached to other areas of the cellular surface, and in some they have been secondarily lost. Stramenopiles represent one of the three major clades in the SAR supergroup, along with Alveolata and Rhizaria.

<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">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">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">Katablepharid</span> Group of algae

The kathablepharids or katablepharids are a group of heterotrophic flagellates closely related to cryptomonads. First described by Heinrich Leonhards Skuja in 1939, kathablepharids were named after the genus Kathablepharis. This genus is corrected to Katablepharis under botanical nomenclature, but the original spelling is maintained under zoological nomenclature. They are single-celled protists with two anteriorly directed flagella, an anterior cytostome for ingesting eukaryotic prey, and a sheath that covers the cell membrane. They have extrusomes known as ejectisomes, as well as tubular mitochondrial cristae.

<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.

Colponema is a genus of single-celled flagellates that feed on eukaryotes in aquatic environments and soil. The genus contains 6 known species and has not been thoroughly studied. Colponema has two flagella which originate just below the anterior end of the cell. One extends forwards and the other runs through a deep groove in the surface and extends backwards. Colponema is a predator that feeds on smaller flagellates using its ventral groove. Like many other alveolates, they possess trichocysts, tubular mitochondrial cristae, and alveoli. It has been recently proposed that Colponema may be the sister group to all other alveolates. The genus could help us understand the origin of alveolates and shed light on features that are ancestral to all eukaryotes.

<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.

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