Parvilucifera

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Parvilucifera
Parvilucifera fmicb-08-01624-g004.png
Parvilucifera spp. (A–C) Sporangia with DAPI-stained nuclei. (D–F) Sporangia with green autofluorescence under blue light excitation.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Myzozoa
Class: Perkinsea
Family: Parviluciferaceae
Genus: Parvilucifera
Norén & Moestrup 1999 [1]
Type species
Parvilucifera infectans
Norén & Moestrup 1999 [1]
Species [2]

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.

Contents

The complex life cycle of Parvilucifera consists of biflagellated zoospores that infect a variety of dinoflagellate species, become intracellular feeders or trophonts, and finally develop into sporangia that generate more zoospores. Parvilucifera species could help control dinoflagellate harmful algal blooms.

Systematics

Etymology

The name of this genus derives from Latin parvus 'small',and lucidus 'shining', referring to the small refractile appearance of the organisms. [1]

History

The genus was first described by biologists Fredrik Norén and Øjvind Moestrup in 1999. It was isolated off the west coast of Sweden. The discovery was made through collections of Dinophysis dinoflagellates from the coast, which contained round bodies assumed to be products of sexual reproduction. After preservation in the refrigerator for two weeks, the dinoflagellates had all died but the round bodies remained. These were further investigated, and later found to be sporangia of a parasitic protist, later described as Parvilucifera infectans . [1]

Initially, it was assumed that the observed zooids would grow into dinoflagellate cells, and there was much debate that sporangia did not arise from parasites. However, similar observations of the round bodies were made with plankton material from the same Swedish coast, which led to further investigation. [1] Through combined examination of light and electron microscopy, alongside DNA sequencing of the emerging sporangia from the zooids, the organism displayed similarities with Perkinsus , a protist belonging to the Alveolata group (containing dinoflagellates, ciliates, apicomplexans and others). The mysterious zooids differed from dinoflagellates and apicomplexans in the ultrastructure of their flagellum, which led to the creation of a separate new phylum, Perkinsozoa, encompassing Perkinsus and the new genus Parvilucifera. [1]

Following the discovery of P. infectans, the next species to be discovered was P. sinerae , [3] the closest relative to P. infectans. Then followed the discovery of P. prorocentri (later moved to another genus), [4] P. rostrata , [5] P. corolla [6] and finally P. multicavata . [2]

Classification

Parvilucifera is a genus of Alveolata, a diverse clade of eukaryotic microbes (protists) within the SAR supergroup. In particular, it belongs to the Perkinsozoa, a clade closely related to dinoflagellates according to molecular phylogenetics. [7] For decades, this genus has been classified within the order Rastrimonadida as part of the Perkinsea class, without assignment to any family-rank taxon. [8] [9] In 2017, a new family Parviluciferaceae was created to accommodate Parvilucifera and two additional perkinsozoan genera: Dinovorax and Snorkelia . [10]

As of 2020, there are four valid species in this genus. Two species, P. infectans and P. sinerae, have long been considered different species, but were later revealed to be the same through a set of genetic, morphological and ultrastructural data. [11] One species, P. prorocentri, was formerly placed in this genus, but was later transferred to a new genus Snorkelia . [10] [2] Species are differentiated from each other through genetic distance and morphology. For instance, P. multicavata differs from the type species P. infectans by a higher number of apertures in their sporangia, although smaller in diameter. [2] P. rostrata differs by the shape and size of the ornamentations covering the sporangium wall. [5] Lastly, P. corolla is distinguished from others by the radial disposition of the zoospores within the maturing sporangium, among other traits such as the tear-drop shape of the zoospores themselves. [6]

Biology and life cycle

Parvilucifera sinerae lifecycle fmicb-12-735815-g004.png
Parvilucifera sinerae infecting its dinoflagellate host

Parvilucifera are single-celled alveolates that behave as endoparasites of dinoflagellates. [1] The overall life cycle of most Parvilucifera species consists of: an infective stage of free-living swimming zoospores, also called zooids; an intracellular feeding stage of trophonts; and the development of a resting sporangium inside the host cell, which in turn generates more zoospores. [12]

Zoospores

Parvilucifera zoospores, also named zooids, are elongate or tear-shaped and have two flagella. They are characterized by a large refractile body in the posterior part of the cell (hence the name Parvilucifera, meaning "small shining"), probably a starch grain, located within a vacuole. They present two unequal flagella: a long anterior one and a shorter posterior one, both arising from the anterior part of the cell. The two flagella are orthogonal, arising close together, each in a cavity. In addition, the cells contain a stretched nucleus extending from the flagellar insertion to the posterior end. [1] As other alveolates, they also present large mitochondria with tubular cristae, numerous cortical alveoli, and an apical complex. [1] Their apical complex is reduced in comparison to that of apicomplexans, and it includes a pseudo-conoid, rhoptry-like and microneme-like vesicles, similar to those observed in Ichthyodinium , Amoebophrya and Perkinsus . [5] Their pseudo-conoid is a 5-membered sheet-like conoid, and the simplest conoid structure discovered so far among alveolates. [1] These structures likely play a role in the infection of cells, because they are homologous to the structures found in apicomplexans, where the apical complex secretes enzymes that allow them to enter the host cell. [5]

The zoospores of each Parvilucifera species are slightly different from each other. Zoospores of P. corolla are teardrop-shaped, while zoospores of P. infectans /P. sinerae are elongated. The average length is approximately 2.9 m and width of the zoospores are similar among the three species. [6] The zoospores of P. rostrata show a rostrum, a proboscis-like structure in the apical region, and are larger in size. [6]

Infection and trophonts

In one species, P. sinerae , the process of infection can follow two different pathways, depending on whether the dinoflagellate host is thecate (i.e. with a protective outer layer of cellulose plates) or athecate. If the dinoflagellate is thecate, then the pathway of infection will be nuclear: the process will follow with the de-attachment of dinoflagellate theca. If the host cell does not have protective plates, then cytoplasmic infection will proceed, indicated by the presence of vacuole-like structures in the cytoplasm and the longer resilience of the host cell. [3]

The endoparasites, once they infect the cell, transform into trophonts and degrade the cytoplasmic contents of the host cell. As the process of feeding continues, the contents of the host cell become entirely degraded or pushed to the outer edges of the cell. As this stage comes to an end, a more or less spherical [1] sporangium develops. [6]

Sporangia

The size of the sporangium is proportional to the size of the host cell. [13] The surface of the sporangium is ornamented with regularly arranged warts, around 0.6–0.8 μm long. It also presents several simple apertures, each covered by an operculum, unlike the smooth-walled sporangia seen in Perkinsus . The sporangium wall has a complex structure, with a thick innermost layer surrounded by a nearly equal in size or slightly thinner opaque layer in which the warts are embedded. As it matures, the sporangium acquires a blackish colour. Zoospores develop within, either in the dead host cell or after the sporangium is released from the host. The zooids escape through the aforementioned apertures. The number of zooids produced by each sporangium depends on its size, but generally around 500 zooids are released, and it takes 5–10 minutes for all zooids to leave. Afterwards, the cytoplasm from where the zooids were abstricted becomes a residual body left in the sporangium, consisting of starch grains, mitochondria, endoplasmic reticulum and a large central nucleus-like area. [1]

Ecology

Habitat

The presence of Parvilucifera, along with other Perkinsozoa, has been demonstrated in fresh water, marine waters, and sediments. [6] P. infectans has been found in coastal Sweden where it was first discovered, especially being commonly found in marine sediment. [12]

Through experimental studies, it has been found that lower salinity levels possibly promote a higher infection rate. [3] Two species, P. infectans and P. sinerae, are able to survive extreme conditions in their sporangium phase, due to the resilience of the host cyst which can protect the zoospores. The sporangia are able to survive cold temperatures for many months. [5]

Host range

All species of Parvilucifera are considered generalist parasites for dinoflagellates, meaning that they are able to infect a wide range of dinoflagellate species. The only exception was a species formerly included in this genus, Snorkelia prorocentri , which specialized in the dinoflagellate Prorocentrum fukuyoi . [6] However, studies are increasingly pointing towards preferences for particular species of dinoflagellates. [12] [5]

Importance in algal blooms

The practical importance of Parvilucifera is a topic of interest, as the genus is demonstrated to be a controlling factor of many harmful algal blooms of dinoflagellates. [1] Dinoflagellate blooms have been known to be harmful to the shellfish industry [1] and responsible for producing potent toxins. [12] Some dinoflagellates are also known to create massive faunal mortality and can even be fatal for humans. [5] [12] Parvilucifera species have a generalist dinoflagellate host range, and thus could serve as negative regulators of dinoflagellate communities. [6] There is research underway to understand the specific host ranges for each species in order to better control dinoflagellate blooms. [12]

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.

The Syndiniales are an order of early branching dinoflagellates, found as parasites of crustaceans, fish, algae, cnidarians, and protists. The trophic form is often multinucleate, and ultimately divides to form motile spores, which have two flagella in typical dinoflagellate arrangement. They lack a theca and chloroplasts, and unlike all other orders, the nucleus is never a dinokaryon. A well-studied example is Amoebophrya, which is a parasite of other dinoflagellates and may play a part in ending red tides. Several MALV groups have been assigned to Syndiniales; recent studies, however, show paraphyly of MALVs suggesting that only those groups that branch as sister to dinokaryotes belong to Syndiniales.

<span class="mw-page-title-main">Rhizophydiales</span> Order of fungi

Rhizophydiales are an important group of chytrid fungi. They are found in soil as well as marine and fresh water habitats where they function as parasites and decomposers.

<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.

<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.

Syndinium is a cosmopolitan genus of parasitic dinoflagellates that infest and kill marine planktonic species of copepods and radiolarians. Syndinium belongs to order Syndiniales, a candidate for the uncultured group I and II marine alveolates. The lifecycle of Syndinium is not well understood beyond the parasitic and zoospore stages.

<i>Katabia</i> Genus of heterotrophic protists

Katabia is a genus of soil-dwelling heterotrophic flagellate cercozoans containing the single species Katabia gromovi, and the only member of family Katabiidae.

<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.

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

<i>Tripos muelleri</i> Species of single-celled organism

Tripos muelleri is a species of dinoflagellates of the genus Tripos.

Ichthyodinium is a monotypic genus of dinoflagellates in the family Dinophysaceae. Ichthyodinium chabelardi (/ɪkθioʊˈdɪniəm/) is currently the sole described species of the genus.

<i>Maullinia</i> Genus of intracellular parasites

Maullinia is a genus of intracellular, phytomyxid parasites found across the Southern Hemisphere though primarily in Chile, The Prince Edward Islands, South Africa, Australia, and New Zealand. These parasites infiltrate the cells of their brown algal hosts via cytoplasmic extensions called plasmodia that divide synchronously, becoming increasingly multi-nucleate and engulfing the host cell organelles as they grow. Eventually, as the plasmodia fill the entire cell volume, the host cells become hypertrophied and grow to 3- 4x their original size, showing up as swollen appendages or galls on the host tissue at a macroscopic level. These swollen regions will burst alongside the mature Maullinia plasmodia, releasing biflagellated zoospores to the inter- and extracellular space to disperse the infection further. Zoospores can come from sporangial plasmodia, as in M. ectocarpii, or from resting spores, as in M. braseltonii.

<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.

<i>Phycophthorum</i> Genus of parasitic protists

Phycophthorum is a monotypic genus of protists that parasitize diatoms, containing the sole species Phycophthorum isakeiti. It was discovered in 2020 in the coastal waters of Norway, as parasites of diatoms belonging to the genus Pleurosigma.

<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.

<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).

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Fredrik Norén; Øjvind Moestrup; Ann-Sofi Rehnstam-Holm (October 1999). "Parvilucifera infectans Noren 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. ISSN   0932-4739. Wikidata   Q56038565.
  2. 1 2 3 4 5 Boo Seong Jeon; Myung Gil Park (27 June 2020). "Parvilucifera multicavata sp. nov. (Alveolata, Perkinsozoa), a New Parasitoid Infecting Marine Dinoflagellates Having Abundant Apertures on the Sporangium". Protist . 171 (4): 125743. doi:10.1016/J.PROTIS.2020.125743. ISSN   1434-4610. PMID   32731120. Wikidata   Q98172104.
  3. 1 2 3 4 Rosa Isabel Figueroa; Esther Garcés; Ramon Massana; Jordi Camp (9 August 2008). "Description, host-specificity, and strain selectivity of the dinoflagellate parasite Parvilucifera sinerae sp. nov. (Perkinsozoa)". Protist . 159 (4): 563–578. doi:10.1016/J.PROTIS.2008.05.003. ISSN   1434-4610. PMID   18693068. Wikidata   Q31170770.
  4. ↑ Mona Hoppenrath; Brian S Leander (1 May 2009). "Molecular phylogeny of Parvilucifera prorocentri (Alveolata, Myzozoa): Insights into perkinsid character evolution". Journal of Eukaryotic Microbiology . 56 (3): 251–256. doi:10.1111/J.1550-7408.2009.00395.X. ISSN   1066-5234. PMID   19527352. Wikidata   Q33467541.
  5. 1 2 3 4 5 6 7 8 Frédéric Lepelletier; Sergey A. Karpov; Sophie Le Panse; Estelle Bigeard; Alf Skovgaard; Christian Jeanthon; Laure Guillou (17 October 2013). "Parvilucifera rostrata sp. nov. (Perkinsozoa), a novel parasitoid that infects planktonic dinoflagellates". Protist . 165 (1): 31–49. doi:10.1016/J.PROTIS.2013.09.005. ISSN   1434-4610. PMID   24334099. Wikidata   Q35066131.
  6. 1 2 3 4 5 6 7 8 9 Albert Reñé; Elisabet Alacid; Rosa Isabel Figueroa; Francisco Rodríguez; Esther Garcés (13 December 2016). "Life-cycle, ultrastructure, and phylogeny of Parvilucifera corolla sp. nov. (Alveolata, Perkinsozoa), a parasitoid of dinoflagellates". European Journal of Protistology . 58: 9–25. doi:10.1016/J.EJOP.2016.11.006. ISSN   0932-4739. PMID   28092806. Wikidata   Q31154927.
  7. ↑ 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.
  8. ↑ 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.
  9. ↑ 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.
  10. 1 2 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.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  11. ↑ Boo Seong Jeong; Seung Won Nam; Sunju Kim; Myung Gil Park (15 March 2018). "Revisiting the Parvilucifera infectans / P. sinerae (Alveolata, Perkinsozoa) species complex, two parasitoids of dinoflagellates" (PDF). Algae. 33 (1): 1–19. doi:10.4490/ALGAE.2018.33.3.6. ISSN   1226-2617. Wikidata   Q124518906.
  12. 1 2 3 4 5 6 Elisabet Alacid; Albert Reñé; Esther Garcés (26 September 2015). "New Insights into the Parasitoid Parvilucifera sinerae Life Cycle: The Development and Kinetics of Infection of a Bloom-forming Dinoflagellate Host". Protist . 166 (6): 677–699. doi:10.1016/J.PROTIS.2015.09.001. ISSN   1434-4610. PMID   26605683. Wikidata   Q40895722.
  13. ↑ Esther Garcés; Elisabet Alacid; Isabel Bravo; Santiago Fraga; Rosa I Figueroa (23 December 2012). "Parvilucifera sinerae (Alveolata, Myzozoa) is a generalist parasitoid of dinoflagellates". Protist . 164 (2): 245–260. doi:10.1016/J.PROTIS.2012.11.004. ISSN   1434-4610. PMID   23266142. Wikidata   Q44566045.
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