{{Short description|Genus of single-celled organisms}} {{Automatic taxobox | image = Bmc evol bio hoppenrath Polykrikos kofoidii extruded nematocyst fig1l.png | image_caption = A light micrograph of ''Polykrikos kofoidii'' showing an extruded nematocyst. Scale bar = 10µm.<ref name=hoppenrath>{{cite journal|doi=10.1186/1471-2148-9-116|pmid=19467154|pmc=2694157|title=Molecular phylogeny of ocelloid-bearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences|journal=BMC Evolutionary Biology|volume=9|page=116|year=2009|last1=Hoppenrath|first1=Mona|last2=Bachvaroff|first2=Tsvetan R|last3=Handy|first3=Sara M|last4=Delwiche|first4=Charles F|last5=Leander|first5=Brian S |doi-access=free |bibcode=2009BMCEE...9..116H }}</ref> | image_alt = A light micrograph of a bullet-shaped cell with a large spiral filament (the extruded nematocyst). | taxon = Polykrikos | authority = Bütschli, 1873 | subdivision_ranks = Species | subdivision = }} [[File:Britannica Dinoflagellata 2-9-Polykrikos.jpg|thumb|upright=1.5|''Polykrikos'', Illustration after Butschli.<br /><small>Encyclopedia Britannica, 1911</small>]] [[File:Polykrikos and Strombidium.jpg|thumb|''Polykrikos'' (left) and ''Strombidium'' (Ciliophora, right) from Tokyo bay, Yokohama.]]
'''''Polykrikos''''' (from Greek "poly" - many, and "krikos" – ring or circle) is one of the genera of family Polykrikaceae that includes athecate pseudocolony-forming dinoflagellates. ''Polykrikos'' are characterized by a sophisticated ballistic apparatus,<ref>{{cite web|url=https://www.nytimes.com/2017/03/31/science/dinoflagellate-video-one-celled-harpooner.html |title=First Clear View of a One-Celled Harpooner in Action |author=James Gorman |date=31 March 2017 |website=NYTimes.com |access-date=26 December 2017}}</ref> named the nematocyst-taeniocyst complex, which allows species to prey on a variety of organisms. ''Polykrikos'' have been found to regulate algal blooms as they feed on toxic dinoflagellates.<ref name="Gavelis et al., 2017">{{cite journal|last1=Gavelis|first1=G.|last2=Wakeman|first2=K.|last3=Ripken|first3=C.|last4=Ozebek|first4=S.|last5=Holstein|first5=T.|last6=Herranz|first6=M.|last7=Keeling|first7=P.|last8=Leander|first8=B.|title=Microbial arms race: Ballistic "nematocysts" in dinoflagellates represent a new extreme in organelle complexity|journal=Science Advances|date=2017|volume=3|issue=3|article-number=e1602552|doi=10.1126/sciadv.1602552|pmid=28435864|pmc=5375639|bibcode=2017SciA....3E2552G }}</ref><ref name="Nagai et al., 2002">{{cite journal|last1=Nagai|first1=S.|last2=Matsuyama|first2=Y.|last3=Takayama|first3=H.|last4=Kotani|first4=Y.|title=Morphology of ''Polykrikos kofoidii'' and ''P. schwartzii'' (Dinophyceae, Polykrikaceae) cysts obtained in culture|journal=Phycologia|volume=41|issue=4|page=319|doi=10.2216/i0031-8884-41-4-319.1|year=2002|bibcode=2002Phyco..41..319N |s2cid=83728508 }}</ref> However, there is also some data available on Polykrikos being toxic to fish.<ref name="Tang et al., 2013">{{cite journal|last1=Tang|first1=Y.Z.|last2=Harke|first2=M.J.|last3=Gobler|first3=C.J.|title=Morphology, phylogeny, dynamics, and ichthyotoxicity of ''Pheopolykrikos hartmannii'' (Dinophyceae) isolates and blooms from New York, USA|journal=J. Phycol.|volume=49|issue=6|pages=1084–1094|doi=10.1111/jpy.12114|year=2013|pmid=27007629 |bibcode=2013JPcgy..49.1084T |s2cid=12140986 }}</ref>
== History of knowledge ==
''Polykrikos'' was first seen in 1868 by Uljanin and was mistakenly considered as a metazoan larva of a turbellarian flatworms. In 1873 Butschili re-examined the specimen and concluded that the cell was an unusual ciliate, and Bergh later, in 1881, clarified ''Polykrikos'' dinoflagellate affinities.<ref>{{cite journal|last1=Taylor|first1=F. J. R.|title=The Biology of Dinoflagellates|journal=Biological Monographs|date=1987|volume=21}}</ref>
== Morphology == ''Polykrikos'' is a colony of zooids (units of a colonial organism) that carry out simultaneous functions of a whole cell.
All ''Polykrikos'' species have: 1) a slightly curved longitudinal furrow, sulcus, extending to posterior end of the organism 2) a loop-shaped acrobase, which is an anterior extension from the sulcus 3) a transverse furrow, cingulum, with the displacement 4) taeniocyst-nematocyst complexes 5) two or four times less the number of nuclei than of zooids, and 6) ability to disassemble into pseudocolonies with fewer zooids and only one nucleus.<ref name="Hoppenrath and Leander, 2007b">{{cite journal|last1=Hoppenrath|first1=M.|last2=Leander|first2=B.S.|title=Morphology and phylogeny of the pseudocolonial dinoflagellates ''Polykrikos lebourae'' and ''Polykrikos herdmanae'' n. sp|journal=Protist|date=2007b|volume=158|issue=2 |pages=209–227|doi=10.1016/j.protis.2006.12.001|pmid=17241813 }}</ref>
The most distinctive trait of this genus is the formation of multinucleated pseudocolonies that consist of an even number of zooids. Each zooid has a pair of flagella (transverse and longitudinal flagella) and has its own transverse groove, cingulum, but zooid longitudinal furrows, sulci, are fused.<ref name="Hoppenrath and Leander, 2007a">{{cite journal|last1=Hoppenrath|first1=M.|last2=Leander|first2=B. S.|title=Character evolution in polykrikoid dinoflagellates.|journal=J. Phycol.|date=2007a|volume=43|issue=2 |pages=366–377|doi=10.1111/j.1529-8817.2007.00319.x|bibcode=2007JPcgy..43..366H |s2cid=16821791 }}</ref> Transverse flagellum has the lateral projections, mastigonemes, and striated strand common to other dinoflagellates.<ref name="Bradbury et al., 1983">{{cite journal|last1=Bradbury|first1=P.C.|last2=Westfall|first2=J.A.|last3=Townsend|first3=J.|title=Ultrastructure of the dinoflagellate ''Polykrikos''. The Nucleus and Its Connections to the Flagellar Apparatus|journal=Journal of Ultrastructure Research|date=1983|volume=85|issue=1|pages=24–32|doi=10.1016/s0022-5320(83)90113-2|pmid=6686618}}</ref> Often ''Polykrikos'' have half the number of nuclei than zooids, and each pair of zooids shares a nucleus. Within the group there is some variation in which organelles are presented, but trichocysts, nematocysts, taeniocysts, mucocysts and plastids have been observed from different members within the taxon.<ref name="Hoppenrath and Leander, 2007a"/>
Cytoplasm of ''Polykrikos'' is characterized by numerous rough endoplasmic reticulum nets, Golgi complexes and vacuoles. ''Polykrikos'' are known to produce ejectile organelles, the extrusomes. One of them is a nematocyst formed in zooids. Another extrusome found within the organism is rod-shaped taeniocyst which is distally located to nematocyst and was earlier mistakenly considered as a nematocyst-precursor.<ref name="Westfall et al., 1983">{{cite journal|last1=Westfall|first1=J. A.|last2=Bradbury|first2=P. C.|last3=Townsend|first3=J.|title=Ultrastructure of the dinoflagellate ''Polykrikos''. Development of the nematocyst-taeniocyst complex and morphology of the site for extrusion|journal=J Cell Sci |date=1983|volume=63|pages=245–261|doi=10.1242/jcs.63.1.245 |pmid=6685130 }}</ref> Together these organelles are forming taeniocyst-nematocyst complex that is thought to be the best synapomorphy for ''Polykrikos'' clade.<ref name="Hoppenrath and Leander, 2007a"/> Golgi-derived vacuoles are shared by both organelles and supply each with molecules needed for its growth along with participating in NTC articulation.<ref name="Westfall et al., 1983"/> Organelles are located in proximity, but lie within different membranes and are separated by a passage, called "chute". The nematocyst is a larger organelle and lies posterior to taeniocyst. Some recent research <ref name="Gavelis et al., 2017" /> have shown that the work of two organelles is coupled, with the taeniocyst adhering to prey, followed by nematocyst discharge leading to prey puncturing and, lastly, retrieving the prey using a tow filament, located on the end of the nematocysts close to posterior vesicle. The tubule, embedded within nematocyst, discharges towards the prey and hypothesized to be used for prey puncturing.
Furthermore, Gavelis et al.<ref name="Gavelis et al., 2017" /> deeply examined NTC morphology and ballistic mechanism that were shown to be fundamentally different from cnidarians, demonstrating nematocysts have evolved independently in single-celled dinoflagellates. Encasing coiled tubule capsule, unlike in cnidarians, is sealed, which forces stylet upon firing first to puncture the capsule from within to free the filament, and only later to pierce the prey. As the tubule passes through the nozzle, it opens the operculum and uncoils after. Ballistics in cnidarians nematocysts is driven by synthesis of osmotic propellant poly gamma glutamate synthase, PgsAA, while in ''Polykrikos'' it is thought to occur due induced pressure as a result of capsular fibre contraction in the capsule wall.<ref name="Gavelis et al., 2017" /> Nucleus is uniquely characterised by a double-layered fibrous cortex that underlines evaginated nuclear envelope; cortex is hypothesized to provide strength and shape to the nucleus, while nuclear evaginations are thought to increase nuclear-cytoplasmic exchange area at cortex perforation sites.<ref name="Bradbury et al., 1983"/>
In ''Polykrikos'', well-defined fibrous ribbons are involved in nuclear-flagellar connections, and anchoring to flagellar apparatus might serve in orientation of the nucleus in relation to flagella during processes of movement, mitosis and cell division.<ref name="Bradbury et al., 1983"/>
== Plastids == There is a variation in nutrient acquisition among ''Polykrikos'' species as some exclusively rely on photosynthesis, some are mixothrophs, while some are obligate heterotrophs which makes ''Polykrikos'' a useful group to study for organellar evolution. Early-branching polykrikoids, ''Polykrikos geminatum'' and ''P. hartmanii'', have three-membrane plastids with triple stacked thylakoids that are indicative of secondary peridinin-type plastids common for dinoflagellates. However, mixothrophic ''P. lebouriae'', phylogenetically nested among heterothropic polykrikoids, has plastids atypical of dinoflagellates. It has two membranes and contain the double-stacked thylakoids that are found in diatoms and haptophytes. However, molecular data analysis by Gavelis et al.<ref name="Gavelis et al., 2015">{{cite journal|last1=Gavelis|first1=G.|last2=White|first2=R. A.|last3=Suttle|first3=C. A.|last4=Keeling|first4=P. J.|last5=Leander|first5=B. S.|title=Single-cell transcriptomics using spliced leader PCR: Evidence for multiple losses of photosynthesis in polykrikoid dinoflagellates|journal=BMC Genomics|date=2015|volume=16|issue=1|page=528 |doi=10.1186/s12864-015-1636-8|pmc=4504456|pmid=26183220 |doi-access=free }}</ref> has demonstrated that ''P. lebouriae'' have peridinin-type plastids that were most likely acquired from ancestral polykrikoids. Transcriptomics analysis demonstrated multiple losses events in polykrikoids that might be explained from energetics and physiological restriction perspectives. Gradual increase in size of ''Polykrikos'' makes the organisms great predators, but increase in body size of single cells is known to result in increased self-shading of chloroplasts and decreased surface area to volume ratio, leading to decreased photosynthetic efficiency. Presence of specialised NTC and large cell size might have triggered multiple losses of photosynthesis.<ref name="Gavelis et al., 2015"/>
== Life cycle of ''P. kofoidii'' == For the genus of ''Polykrikos'', detailed data is available on reproduction of a type species (holotype) ''P. kofoidii'', whose life cycle resembles general dinoflagellate cycle as vegetative cells form gametes that fuse to form a diploid (2n) zygote that could encyst, but pseudocolonial nature adds a number of peculiarities to the ''Polykrikos'' development.<ref name="Tillmann and Hoppenrath 2013">{{cite journal|last1=Tillmann|first1=U.|last2=Hoppenrath|first2=M.|title=Life Cycle of the pseudocolonial dinoflagellate ''Polykrikos kofoidii'' (Gymnodiniales, Dinoflagellata)|journal=Journal of Phycology|date=2013|volume=49|issue=2|pages=298–317|doi=10.1111/jpy.12037|pmid=27008517|bibcode=2013JPcgy..49..298T |s2cid=30674349 }}</ref>
When organisms were well-fed, they appeared as 4-zooid-2-nuclei pseudocolonies, and during vegetative reproduction doubled number of zooids followed by nuclei division leading to 8-zooid-4-nuclei stage with further transverse binary division into two 4-zooid-2-nuclei ''Polykrikos''. Gamete formation was particular as pseudocolony produces 4 gametes of different sizes and morphologies than vegetative cells. Vegetative form doubled zooids and subsequently split into four gametes of a 2-zooid-1-nucleus form. Two gametes further paired up with their ventral sides and fused forming a planozygote. For ''P. kofoidii'' two copulation finger-shaped structures were observed in gametes that are presumably involved in gamete contact and fusion, but more data is needed to confirm this. The ventrally fused gametes required a complex rearrangement of eight flagella and formation of sulci and cinguli. The 4-zooid planozygote had only one nucleus and had two developmental pathways depending on food availability. Under starvation conditions the planozygote disassembled into two 2-zooid with one lacking nucleus, but further fate was not examined. Under culture conditions most organisms undergone meiosis and directly entered vegetative cycle. Very few planozygotes went through a resting cyst stage. The cyst stage persisted for 1 month, which is considered as a relatively short period in comparison to other dinoflagellates, which obligate dormancy period may reach up to 6 month. The duration of encystment is associated with ecological foraging strategies. Short dormancy period could facilitate rapid cycling between life cycle stages that could be beneficial to heterotrophic species in case of fluctuating food availability. However, possibility of chemical signalling involved in cyst hatching for ''Polykrikos'' is yet to be determined.
Germling, a single zooid cell, emerging from the cyst, had a unique development that has never been documented for any free-living dinoflagellate. Its morphology clearly went from a 1-zooid-1-nucleus, over a 2-zooid-1-nucleus, and a 4-zooid-1-nucleus into the 4-zooid-2-nucleus stage. This data raises the question whether such hatching pattern may reflect the ''Polykrikos'' pseudocolonies phylogeny.<ref name="Tillmann and Hoppenrath 2013"/>
== Habitat and ecology (niche, food) ==
All known ''Polykrikos'' species are found in marine environments. A majority of species are planktonic with theexception of ''Polykrikos lebouriae'' and ''Polykrikos herdmanae'' that are found in benthic habitat.<ref name="Hoppenrath and Leander, 2007b"/> There is also variation in feeding ecology as some species have plastids and can use photosynthesis to obtain nutrients but often happen to be mixotrophs (''P. barnegatensis, P. lebouriae, P tanit, P. hartmannii''). Only one species is known to be exclusively autotrophic (''P. geminatum''), while some lack the plastid and are completely heterotrophic (''P. grassei, P. herdmanae, P. kofoidii'' and ''P. schwartzii''),.<ref name="Lee et al., 2015">{{cite journal|last1=Lee|first1=M. J.|last2=Jeong|first2=H. J.|last3=Lee|first3=K. H.|last4=Jang|first4=S. H.|last5=Kim|first5=J. H.|last6=Kim|first6=K. Y.|title=Mixotrophy in the nematocyst–taeniocyst complex-bearing phototrophic dinoflagellate ''Polykrikos hartmannii''|journal=Harmful Algae|date=2015|volume=49|pages=124–132|doi=10.1016/j.hal.2015.08.006}}</ref><ref name="Hoppenrath and Leander, 2007a"/>
''Polykrikos hartmannii'' is a phototrophic dinoflagellate and has been reported in waters of Canada,<ref name="Hoppenrath et al., 2010">{{cite journal|last1=Hoppenrath|first1=M.|last2=Yubuki|first2=N.|last3=Bachvaroff|first3=S.|last4=Leander|first4=B. S.|title=Re-classification of ''Pheopolykrikos hartmannii'' as ''Polykrikos'' (Dinophyceae) based partly on the ultrastructure of complex extrusomes|journal=Eur. J. Protistol.|date=2010|volume=46|issue=1 |pages=29–37|doi=10.1016/j.ejop.2009.08.003|pmid=19767184}}</ref> USA, Mexico, China, India, Japan, and Korea.<ref name="Tang et al., 2013"/><ref name="Lee et al., 2015"/> ''P. hartmanii'' feeds on algal species by engulfment after anchoring a prey using a nematocyst-taeniocyst complex (later referred to as NTC).<ref name="Lee et al., 2015"/> Tang et al.<ref name="Tang et al., 2013"/> observed a ''P. hartmannii'' bloom that caused 100% mortality in juvenile sheepshead minnows (''Cyprinodon variegates'') within 24 hours suggesting ''P. hartmannii'' is an ichthyotoxic, harmful alga. ''P.hartmannii'' feeds on chain-forming dinoflagellates ''Cochlodinium polykrikoides'' and ''Gymnodinium catenatum'' that are also known to cause fish mortality, and therefore ''P. hartmannii'' is thought to have enzymes that detoxify toxins produced by these prey dinoflagellates.<ref name="Lee et al., 2015"/> Also, a comparison of three ''Polykrikos'' species feeding revealed that species differ in their prey preference, and some are more specialized than the other, such that ''P. hartmanii'' preying is less diverse (fed on 2 prey species) than of ''P. kofoidii'' and ''P. lebouriae'', which fed on 14 different algal species.<ref name="Lee et al., 2015"/>
Predation by heterotrophic ''Polykrikos'' became a great topic of interest as some of the organisms graze on dinoflagellates that cause toxic blooms. High predation impact by ''Polykrikos schwartzii'' Butschili on toxic dinoflagellate ''Alexandrium tamarense'' (Lebour) Balech was reported in Argentina, while ''Polykrikos kofoidii'' Chatton was controlling ''Gymnodium catenatum'' Graham in Portuguese and Japanese coastal waters.<ref name="Nagai et al., 2002" /> ''G. catenatum'' is one of the species causing paralytic shellfish poisoning (PSP) and is found in waters of Australia, Japan, Mexico and Spain.<ref name="Matsuyama et al., 1999">{{cite journal|last1=Matsuyama|first1=Y|last2=Miyamoto|first2=M|last3=Kotani|first3=Y|title=Grazing impacts of the heterotrophic dinoflagellate ''Polykrikos kofoidii'' on a bloom of ''Gymnodinium catenatum''|journal=Aquat Microb Ecol|date=1999|volume=17|pages=91–98|doi=10.3354/ame017091|doi-access=free}}</ref> Observations of feeding behaviour suggest ''P. kofoidii'' initially displayed looping swimming behaviour in close proximity to its prey followed by discharge of a nematocyst, pull of the prey into the body through posterior sulcus and final engulfment of the prey.<ref name="Matsuoka et al., 2000">{{cite journal|last1=Matsuoka|first1=K.|last2=Cho|first2=H. J.|last3=Jacobson|first3=D. M.|title=Observation of the feed ing behaviour and growth rates of the heterotrophic dinoflagellate, ''Polykrikos kofoidii'' (Polykrikaceae. Dinophyceae) 39: 82- 86.|journal=Phycologia|date=2000|volume=39|pages=82–86|doi=10.2216/i0031-8884-39-1-82.1|s2cid=86293920 }}</ref> PSP raises socio-economic-environmental concerns as it affects the health of both marine mammals and humans, and the regulation mechanism of toxic microalgae population by ''P.kofoidii'' could be important in environmental monitoring and health hazard elimination.
== Practical importance == Predation of toxic microalgae by heterotrophic dinoflagellates is one of the factors controlling the algal blooms. ''Polykrikos'' are known to modulate populations of dinoflagellates like ''Alexandrium tamarense'',<ref name="Gavelis et al., 2017" /><ref name="Nagai et al., 2002" /> and G. catenatum,<ref name="Jeong et al., 2003">{{cite journal|last1=Jeong|first1=H.|last2=Park|first2=K.|last3=Kim|first3=J.|last4=Kang|first4=H.|last5=Kim|first5=C.|last6=Choi|first6=H.,...|last7=Park|first7=M.|title=Reduction in the toxicity of the dinoflagellate ''Gymnodinium catenatum'' when fed on by the heterotrophic dinoflagellate ''Polykrikos kofoidii''.|journal=Aquatic Microbial Ecology|date=2003|volume=31|pages=307–312|doi=10.3354/ame031307|doi-access=free}}</ref> which are among prevalent agents of toxic algal blooms. Such heterothrophic polykrikoids may not only cut down on the toxicity levels induced by their prey in marine food webs, but can cease the toxic blooms and could be used in bioremediation.<ref name="Jeong et al., 2003"/> Thus, reduction in water toxicity may help regulate the balance of marine food webs and decrease mortality rates of finfish, marine mammals, and sea birds. Further studies on molecular mechanisms of detoxification by ''Polykrikos'' maybe helpful in biomedical and environment-monitoring fields.
However, some ''Polykrikos'' pose a health risk to certain fishes, while the bloom-regulating ones are often preyed on by marine invertebrates, like amphipods, which would return the toxins back into the food web.<ref name="Jeong et al., 2003"/> Some polykrikoid population monitoring and investigation of toxin dynamics inside the body of grazers could provide better understanding of plankton-based food webs, estimate degrees of poisoning in ecosystems and propose potential toxin elimination routes.
== List of species == Currently the following 10 species are accepted taxonomically:<ref name="Guiry (2002)">{{cite web|last1=Guiry|first1=M. D.|title=Polykrikos Butschli, 1873|url=http://www.algaebase.org|website=Algaebase|access-date=February 20, 2017}}</ref> * ''Polykrikos barnegatensis'' G.W.Martin, * ''Polykrikos geminatus'' (F.Schütt) D.X.Qiu & Senjie Lin, * ''Polykrikos grassei'' Lecal, * ''Polykrikos hartmannii'' W.Zimmermann, * ''Polykrikos herdmaniae'' Hoppenrath & Leander, * ''Polykrikos kofoidii'' Chatton, * ''Polykrikos lebouriae'' Herdman, * ''Polykrikos schwartzii'' Bütschli, * ''Polykrikos tanit'' Reñé, * ''Polykrikos tentaculatus'' O.Wetzel
== References == {{Reflist}}
{{Taxonbar|from=Q5550547}}
Category:Dinoflagellate genera Category:Bioluminescent dinoflagellates Category:Gymnodiniales