| Parvilucifera | |
|---|---|
 | |
| Parvilucifera spp. (A–C)Sporangia withDAPI-stainednuclei. (D–F) Sporangia withgreen autofluorescence under blue light excitation. | |
Scientific classification | |
| 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 ofmarinealveolates that behave asendoparasites ofdinoflagellates. It was described in 1999 by biologists Fredrik Norén andØjvind Moestrup, who identified the genus among collections ofDinophysis dinoflagellates off the coast ofSweden. Initially mistaken for products ofsexual reproduction, the round bodies found within these collections were eventually recognized assporangia, spherical structures that generatezoospores of a parasitic protist. This organism was later identified asP. infectans, thetype species. The examination of this organism and its close genetic relationship toPerkinsus led to the creation of thePerkinsozoa phylum within theAlveolata group.
The complexlife cycle ofParvilucifera consists ofbiflagellated zoospores that infect a variety of dinoflagellate species, become intracellular feeders ortrophonts, and finally develop into sporangia that generate more zoospores.Parvilucifera species could help control dinoflagellateharmful algal blooms.
The name of this genus derives from Latin parvus 'small' and lucidus 'shining', referring to the smallrefractile appearance of the organisms.[1]
The genus was first described bybiologists Fredrik Norén andØjvind Moestrup in 1999. It was isolated off the westcoast ofSweden. The discovery was made throughcollections ofDinophysisdinoflagellates from the coast, which contained round bodies assumed to be products ofsexual 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 asParvilucifera 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 oflight andelectron microscopy, alongsideDNA sequencing of the emerging sporangia from the zooids, the organism displayed similarities withPerkinsus, a protist belonging to theAlveolata 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, encompassingPerkinsus and the newgenusParvilucifera.[1]
Following the discovery ofP. infectans, the next species to be discovered wasP. sinerae,[3] the closest relative toP. infectans. Then followed the discovery ofP. prorocentri (later moved to another genus),[4]P. rostrata,[5]P. corolla[6] and finallyP. multicavata.[2]
Parvilucifera is a genus ofAlveolata, a diverseclade of eukaryotic microbes (protists) within theSAR supergroup. In particular, it belongs to thePerkinsozoa, a clade closely related todinoflagellates according tomolecular phylogenetics.[7] For decades, this genus has been classified within theorderRastrimonadida as part of thePerkinsea class, without assignment to anyfamily-ranktaxon.[8][9] In 2017, a new familyParviluciferaceae was created to accommodateParvilucifera and two additional perkinsozoan genera:Dinovorax andSnorkelia.[10]
As of 2020, there are four valid species in this genus. Two species,P. infectans andP. sinerae, have long been considered different species, but were later revealed to be the same through a set of genetic, morphological andultrastructural data.[11] One species,P. prorocentri, was formerly placed in this genus, but was later transferred to a new genusSnorkelia.[10][2] Species are differentiated from each other through genetic distance and morphology. For instance,P. multicavata differs from the type speciesP. 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]
Parvilucifera aresingle-celledalveolates that behave asendoparasites ofdinoflagellates.[1] The overalllife cycle of mostParvilucifera species consists of: an infective stage of free-living swimmingzoospores, also called zooids; an intracellular feeding stage oftrophonts; and the development of a restingsporangium inside the host cell, which in turn generates more zoospores.[12]
Parvilucifera zoospores, also named zooids, are elongate or tear-shaped and have two flagella. They are characterized by a largerefractile body in theposterior part of the cell (hence the nameParvilucifera, meaning "small shining"), probably a starch grain, located within avacuole. They present two unequal flagella: a longanterior 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 stretchednucleus extending from the flagellar insertion to the posterior end.[1] As other alveolates, they also present largemitochondria with tubularcristae, numerouscortical alveoli, and anapical complex.[1] Their apical complex is reduced in comparison to that of apicomplexans, and it includes a pseudo-conoid,rhoptry-like andmicroneme-like vesicles, similar to those observed inIchthyodinium,Amoebophrya andPerkinsus.[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 arehomologous to the structures found in apicomplexans, where the apical complex secretes enzymes that allow them to enter the host cell.[5]
The zoospores of eachParvilucifera species are slightly different from each other. Zoospores ofP. corolla are teardrop-shaped, while zoospores ofP. 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 ofP. rostrata show a rostrum, a proboscis-like structure in the apical region, and are larger in size.[6]
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 ofcellulose plates) or athecate. If the dinoflagellate is thecate, then the pathway of infection will benuclear: the process will follow with the de-attachment of dinoflagellate theca. If the host cell does not have protective plates, thencytoplasmic infection will proceed, indicated by the presence ofvacuole-like structures in the cytoplasm and the longer resilience of the host cell.[3]
The endoparasites, once they infect the cell, transform intotrophonts and degrade thecytoplasmic 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]
The size of thesporangium 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 inPerkinsus. 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, thecytoplasm from where the zooids were abstricted becomes a residual body left in the sporangium, consisting ofstarch grains,mitochondria,endoplasmic reticulum and a large centralnucleus-like area.[1]
The presence ofParvilucifera, along with otherPerkinsozoa, has been demonstrated infresh water,marine waters, and sediments.[6]P. infectans has been found in coastalSweden where it was first discovered, especially being commonly found in marine sediment.[12]
Through experimental studies, it has been found that lowersalinity levels possibly promote a higher infection rate.[3] Two species,P. infectans andP. sinerae, are able to survive extreme conditions in their sporangium phase, due to the resilience of the hostcyst which can protect the zoospores. The sporangia are able to survive cold temperatures for many months.[5]
All species ofParvilucifera are consideredgeneralistparasites fordinoflagellates, 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 dinoflagellateProrocentrum fukuyoi.[6] However, studies are increasingly pointing towards preferences for particular species of dinoflagellates.[12][5]
The practical importance ofParvilucifera is a topic of interest, as the genus is demonstrated to be a controlling factor of manyharmful algal blooms ofdinoflagellates.[1] Dinoflagellate blooms have been known to be harmful to theshellfish 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]