''Haplozoon'' (/hæploʊ’zoʊən/) are unicellular endo-parasites, primarily infecting maldanid

polychaete Polychaeta () is a paraphyletic class of generally marine annelid worms, commonly called bristle worms or polychaetes (). Each body segment has a pair of fleshy protrusions called parapodia that bear many bristles, called chaetae, which are made ...

s. They belong to Dinoflagellata but differ from typical dinoflagellates. Most dinoflagellates are free-living and possess two

flagella A flagellum (; ) is a hairlike appendage that protrudes from certain plant and animal sperm cells, and from a wide range of microorganisms to provide motility. Many protists with flagella are termed as flagellates. A microorganism may have fro ...

. Instead, ''Haplozoon'' belong to a 5% minority of parasitic dinoflagellates that are not free-living. Additionally, the ''Haplozoon'' trophont stage is particularly unique due to an apparent lack of flagella. The presence of flagella or remnant structures is the subject of ongoing research. At first glance, ''Haplozoon'' also do not appear unicellular – in fact they were originally classified as a possible transitional stage between

protist A protist () is any eukaryotic organism (that is, an organism whose cells contain a cell nucleus) that is not an animal, plant, or fungus. While it is likely that protists share a common ancestor (the last eukaryotic common ancestor), the e ...

s and

multicellular organism A multicellular organism is an organism that consists of more than one cell, in contrast to unicellular organism. All species of animals, land plants and most fungi are multicellular, as are many algae, whereas a few organisms are partially uni ...

s.Shumway, W. (1924). The genus ''Haplozoon'', Dogiel. Observations on the life history and systematic position. ''The Journal of Parasitology, 11''(2), 59-74. They have more recently been classified as compartmentalized

syncytia A syncytium (; plural syncytia; from Greek: σύν ''syn'' "together" and κύτος ''kytos'' "box, i.e. cell") or symplasm is a multinucleate cell which can result from multiple cell fusions of uninuclear cells (i.e., cells with a single nucleus) ...

– single cells with multiple nuclei that have been subdivided by internal membranes.Leander, B., Saldarriaga, J., & Keeling, P. (2002). Surface morphology of the marine parasite ''Haplozoon axiothellae'' Siebert (Dinoflagellata). ''European Journal of Protistology, 38''(3), 287–297. doi: 10.1078/0932-4739-00882 Their life cycle is also largely unknown; while there is a well-observed adult trophont stage, understanding of other life stages is speculative at best. There is a single published case of ''Haplozoon'' infecting an appendicularian.Cachon J. (1964). Contribution a l’étude des Péridiniens parasites. Cytologie. Cycles évolutifs. ''Ann. Sci. Nat. Zool. 12'': 1-158. Otherwise, they are almost exclusively documented as infecting

Maldanidae Maldanidae is a family of more than 200 species of marine polychaetes commonly known as bamboo worms or maldanid worms. They belong to the order Capitellida, in the phylum Annelida. They are most closely related to family Arenicolidae, and toget ...

, and the extent to which they are an appendicularian parasite has not been investigated.

Etymology

Haplozoon derives from two Greek words: ''haploos'' meaning “single, or simple” and ''zoion'' meaning “animal”. When they were first discovered, they were initially placed within Mesozoa, a group of highly reduced worm-like parasitic invertebrates. Therefore, the genus name ''Haplozoon'' means “simple animal”.

History of Knowledge

The type species ''Haplozoon armatum'' was discovered by Russian zoologist Valentin Dogiel in 1906. Dogiel initially described ''Haplozoon'' as belonging to the

Mesozoa The Mesozoa are minuscule, worm-like parasites of marine invertebrates. Generally, these tiny, elusive creatures consist of a somatoderm (outer layer) of ciliated cells surrounding one or more reproductive cells. A recent study recovered Mesoz ...

, and established a new mesozoan class, the Catenata. A series of early protistologists continued to fine-tune the taxonomical position of ''Haplozoon'' for a number of years. The following year, the French biologist

Édouard Chatton Édouard Chatton (; 11 October 1883 – 23 April 1947) was a French biologist who first characterized the distinction between the prokaryotic and eukaryotic cellular types. Chatton coined the terms and published them first in his 1937 paper ' ...

indicated similarities between ''Haplozoon'' and ''

Blastodinium ''Blastodinium'' (also known as ''Blastodiniphycaea'') is a diverse genus of dinoflagellates and important parasites of planktonic copepods. They exist in either a parasitic stage, a trophont stage, and a dinospore stage. Although morphologicall ...

'' in 1907. Later, in 1911, the German naturalist Franz Poche created a new protozoan class – the Haplozooidea. And again in 1920, Chatton created a new family (Haplozoonidae) for the genus, of the order Gymnodinida (modern syn.

Gymnodiniales The Gymnodiniales are an order of dinoflagellates, of the class Dinophyceae. Members of the order are known as gymnodinioid or gymnodinoid (terms that can also refer to any organism of similar morphology). They are athecate, or lacking an armo ...

). By the 1970s ''Haplozoon'' had been moved from the Gymnodiniales to the order of Blastodiniales.Siebert, A. (1973). A description of ''Haplozoon axiothellae'' n. sp., an endosymbiont of the polychaete ''Axiothellae rubrocincta''. ''Journal of Phycology, 9''(2), 185-190. doi: 10.1111/j.1529-8817.1973.tb04077.x Our modern understanding of ''Haplozoon'' is limited. There were a series of species discoveries in the early 1900s, however these publications lack the modern techniques that would be mandatory today (e.g.

transmission electron microscopy Transmission electron microscopy (TEM) is a microscopy technique in which a beam of electrons is transmitted through a specimen to form an image. The specimen is most often an ultrathin section less than 100 nm thick or a suspension on a ...

, scanning electron microscope,

molecular sequencing In genetics and biochemistry, sequencing means to determine the primary structure (sometimes incorrectly called the primary sequence) of an unbranched biopolymer. Sequencing results in a symbolic linear depiction known as a sequence which succi ...

, etc.). Only 5 species of ''Haplozoon'' have been sufficiently described by modern standards: ''Haplozoon axiothellae,''Siebert, A., & West, J. (1974). The fine structure of the parasitic dinoflagellate ''Haplozoon axiothellae''. ''Protoplasma, 81''(1), 17-35. doi: 10.1007/BF02055771 ''Haplozoon praxillellae,''Rueckert, S., & Leander, B. (2008). Morphology and molecular phylogeny of ''Haplozoon praxillellae'' n. sp. (Dinoflagellata): a novel intestinal parasite of the maldanid polychaete ''Praxillella''. ''European Journal of Protistology, 44''(4), 299-307. doi: 10.1016/j.ejop.2008.04.004 ''Haplozoon ezoense,''Wakeman, K., Yamaguchi, A., & Horiguchi, T. (2018). Molecular phylogeny and morphology of ''Haplozoon ezoense'' n. sp. (Dinophyceae): A parasitic dinoflagellate with ultrastructural evidence of remnant non-photosynthetic plastids. ''Protist'', 169(3), 333-350. doi: 10.1016/j.protis.2018.04.008 ''Haplozoon gracile,'' ''and Haplozoon pugnus.'' In some cases, insufficient information has resulted

nomen nudum In taxonomy, a ''nomen nudum'' ('naked name'; plural ''nomina nuda'') is a designation which looks exactly like a scientific name of an organism, and may have originally been intended to be one, but it has not been published with an adequate desc ...

. This is the case for ''H. inerme'', and ''H. hirsutum''. In many cases, species of ''Haplozoon'' are also phantom species. Phantom species are those that were perhaps adequately described at first, but have not been seen since their initial discovery. The three types of haplozoan compartments were originally named with the suffix -cyte (trophocyte, gonocyte, and sporocyte). Within biology, the -cyte suffix historically denotes different cell types (osteocyte, lipocyte, erythrocyte). Because ''Haplozoon'' were thought to be multicellular when originally described, the haplozoan compartments were named as if they are separate cells. When it was determined that ''Haplozoon'' were not multicellular, and in fact a compartmentalized syncytium, the three compartments were renamed with the suffix -mere (trophomere, gonomere, sporomere), to accurately portray them as belonging to a single cell.

Habitat and ecology

''Haplozoon'' are

obligate parasite An obligate parasite or holoparasite is a parasitic organism that cannot complete its life-cycle without exploiting a suitable host. If an obligate parasite cannot obtain a host it will fail to reproduce. This is opposed to a facultative parasi ...

s. They are almost exclusively found in the gut of maldanid marine worms, with one study documenting a ''Haplozoon'' parasite infecting an appendicularian. Each trophont has a stylet, which it uses to pierce the gut lining of the host worm. It is unclear if the stylet is used only for anchoring the parasite, or if it is involved in feeding as well. If ''Haplozoon'' do use their stylet to feed, this would be referred to as

myzocytosis Myzocytosis (from Greek: myzein, (') meaning "to suck" and kytos (') meaning "container", hence referring to "cell") is a method of feeding found in some heterotrophic organisms. It is also called "cellular vampirism" as the predatory cell pierces ...

, and commonly referred to as “cellular vampirism”. This is an established feeding method among other alveolate parasites. Another possible feeding strategy is that the parasite absorbs nutrients that are released as the host worm digests food. This feeding strategy is referred to as

pinocytosis In cellular biology, pinocytosis, otherwise known as fluid endocytosis and bulk-phase pinocytosis, is a mode of endocytosis in which small molecules dissolved in extracellular fluid are brought into the cell through an invagination of the cell ...

, a form of endocytosis where nutrients suspended in the fluid if the host's gut are absorbed through the

cell membrane The cell membrane (also known as the plasma membrane (PM) or cytoplasmic membrane, and historically referred to as the plasmalemma) is a biological membrane that separates and protects the interior of all cells from the outside environment (t ...

of the parasite. The exterior of ''Haplozoon'' cells are covered by barbs that present as fine hair-like structures that might function in surface mediated nutrition similar to the

microtriches Microtriches (singular microtrix) are the highly specialized microvilli covering the entire surface of the tegument of cestodes. They are fine hair-like filaments distributed throughout the surface of the body, both unique to and ubiquitous among ...

cestoda Cestoda is a class of parasitic worms in the flatworm phylum (Platyhelminthes). Most of the species—and the best-known—are those in the subclass Eucestoda; they are ribbon-like worms as adults, known as tapeworms. Their bodies consist of ...

. With few exceptions, most descriptions of ''Haplozoon'' are from European coastlines. ''Haplozoon clymenellae'' is from the Atlantic coast of North America, while ''H. axiothellae'', and ''H. praxillellae'' have been found on the Pacific coast of Washington, US and British Columbia, Canada. ''H. ezoense, H. gracile, and H. pugnus'' were discovered on the coast of Japan. There are currently no recorded observations from the tropics or the southern hemisphere, and consequently little is known about its biogeographical distribution.

Description of the organism

Morphology

What makes ''Haplozoon'' unique among dinoflagellates is their functional multicellularity. ''H. axiothellae'' cells are composed of a series of compartments, which give them the appearance of multicellularity. At minimum all ''Haplozoon'' species consist of a single row of compartments, with mature cells of some species containing two or more rows of compartments at the posterior of their cell. These compartments are specialized for different functions, such as host attachment, feeding and reproduction. ''Haplozoon'' were originally described as having 2-26 “cells”, however the degree of compartmentalization varies by species. Species also vary in size, but the most well-studied (''H. axiothellae'') is described as being 40-175 μm in length, and 15-40 μm wide. The exterior of ''Haplozoon'' cells are covered in amphiesmal projections (syn. thecal barbs). The ''Haplozoon'' trophont (i.e. the stage that parasitizes the host) has 3 types of compartments: (1) a trophomere used to attach to the host, (2) repeating gonomeres that compose the majority of the cell length, and (3) sporomeres which develop from mature gonomeres. The anterior-most compartment of the cell is the trophomere, larger than the gonomeres that are immediately posterior to it. The rear most compartments are referred to as sporomeres, and depending on the species of ''Haplozoon'', sporomeres may remain in single file (e.g. ''H. lineare''), form double rows (e.g. ''H. axiothellae'') or even multiple rows (e.g. ''H. clymenellae''). All three compartment types appear granular under

light microscopy Microscopy is the technical field of using microscopes to view objects and areas of objects that cannot be seen with the naked eye (objects that are not within the resolution range of the normal eye). There are three well-known branches of micr ...

, due to starch granules in their

cytoplasm In cell biology, the cytoplasm is all of the material within a eukaryotic cell, enclosed by the cell membrane, except for the cell nucleus. The material inside the nucleus and contained within the nuclear membrane is termed the nucleoplasm. ...

. In ''H. axiothellae'', cytoplasic granularity increase from anterior to posterior, concentrating in the sporomeres. It is thought that starch accumulation in the sporomeres provides a reserve of energy for a subsequent life stage to survive in a marine environment without a host. ''Haplozoon'' lack visible flagella, where traditional dinoflagellates have two – one transverse and one longitudinal. However, ''H. axiothellae'' possesses a longitudinal row of ventral pores along their surface, and confocal scanning laser microscopy (CLSM) data have revealed two basal bodies embedded in the plasma membrane of each compartment. These basal bodies are found along the cell's ventral surface, aligned with the cell's ventral pores. Taken together, these data indicate that ''Haplozoon'' possess the vestiges of the flagellar system present in most dinoflagellates. This is consistent with the prediction of a subsequent life stage possessing flagella, because eukaryotic flagella require basal bodies to anchor and organize flagellar microtubules. CLSM data also show that the microtubules of the

cytoskeleton The cytoskeleton is a complex, dynamic network of interlinking protein filaments present in the cytoplasm of all cells, including those of bacteria and archaea. In eukaryotes, it extends from the cell nucleus to the cell membrane and is co ...

originate from these basal bodies, and function as microtubule organizing centers. The trophomere attaches to the gut lining of the host by means of its stylet and adhesive disc. Some species of ''Haplozoon'' possess a single stylet (''H. ezoense''), whereas others are known to have multiple (reserve) stylets within the trophomere (''H. axiothellae, H. praxillellae''). Some species also appear to have “arms” that extend from the trophomere. CLSM data reveal a basket of microtubules lining the interior of the trophomere. This basket of microtubules provides the cytoskeletal structure that supports the dynamic movement and behavior of the trophomere, with microtubules especially concentrated in the adhesive disk. Early transmission electron microscopy (TEM) briefly describes 3 layers of the cellular membrane. They describe a single continuous outer layer equivalent to a cell membrane, with two subsequent layers below of compressed “thecal vesicles”. Today these “thecal vesicles” are known as

alveoli Alveolus (; pl. alveoli, adj. alveolar) is a general anatomical term for a concave cavity or pit. Uses in anatomy and zoology * Pulmonary alveolus, an air sac in the lungs ** Alveolar cell or pneumocyte ** Alveolar duct ** Alveolar macrophage * M ...

, or amphiesmal vesicles. The divisions between gonomeres are described as outer continuous membranes and flattened vesicles but pressed so closely together that they are impossible to distinguish. The divisions between compartments are now understood to be created by interlocking amphiesmal vesicles rather than cellular membranes. This solidified the description of ''Haplozoon'' as compartmentalized syncytia, rather than multicellular organisms. However, there is evidence of eventual plasma membrane formation at the rear of the cell, where plasma membrane appears to form along the layers of alveoli separating compartments. This indicates that sporomeres do eventually develop their own plasma membranes through

cytokinesis Cytokinesis () is the part of the cell division process during which the cytoplasm of a single eukaryotic cell divides into two daughter cells. Cytoplasmic division begins during or after the late stages of nuclear division in mitosis and mei ...

, which would be necessary for sporomeres to break away and survive independently from the adult trophont. All compartments contain their own nuclei, with some gonomeres being binucleate and some sporomeres being quadrinucleate. Nuclei are nearly always in some stage of division, with robust spindle fibres present in virtually all of them. The nuclei of ''Haplozoon'' have thick

chromosome A chromosome is a long DNA molecule with part or all of the genetic material of an organism. In most chromosomes the very long thin DNA fibers are coated with packaging proteins; in eukaryotic cells the most important of these proteins ar ...

s, typical of Dinokaryota.

Mitochondria A mitochondrion (; ) is an organelle found in the cells of most Eukaryotes, such as animals, plants and fungi. Mitochondria have a double membrane structure and use aerobic respiration to generate adenosine triphosphate (ATP), which is used ...

are mainly located below the amphiesmal vesicles towards the outside of the cell and possess tubular cristae. TEM sections have revealed multiple triple membrane-bound organelles within the gonomeres. They are roughly spherical and range in size from 200 nm – 750 nm. They appear like relic non-photosynthetic

plastid The plastid (Greek: πλαστός; plastós: formed, molded – plural plastids) is a membrane-bound organelle found in the cells of plants, algae, and some other eukaryotic organisms. They are considered to be intracellular endosymbiotic cyan ...

s, which have been found among other members of

Myzozoa Myzozoa is a grouping of specific phyla within Alveolata, that either feed through myzocytosis, or were ancestrally capable of feeding through myzocytosis. Many protozoan orders are included within Myzozoa. It is sometimes described as a ph ...

(

apicomplexa The Apicomplexa (also called Apicomplexia) are a large phylum of parasitic alveolates. Most of them possess a unique form of organelle that comprises a type of non-photosynthetic plastid called an apicoplast, and an apical complex structure. Th ...

ns as well as dinoflagellates). This is consistent with our understanding that some lineages of dinoflagellates have experienced plastid loss as they evolved.Saldarriaga, J., Taylor, F., Keeling, P., & Cavalier-Smith, T. (2001). Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. ''Journal of Molecular Evolution'', 53(3), 204–213. doi: 10.1007/s002390010210 This discovery in ''Haplozoon'' only provides ultrastructure evidence for these remnant plastids; no research has been published to assess plastid genes and any associated metabolic pathways.

Life cycle

Very little is confirmed about the ''Haplozoon'' life cycle; the only life-stage that is known is the trophont. Given similarities with other dinoflagellate parasites, it is hypothesized that the known trophont stage is the “adult”. It is presumed that the sporomeres are what allow the organism to reproduce, but this has not been shown definitively. It is well-documented that sporomeres eventually detach from the trophont, thought to be released through the anus of the host, and into the marine environment where the sporomere would become a motile life stage that has yet to be described. Once in the marine environment, the dinospores can be ingested by a new host, and subsequently develop into an adult trophont and attach themselves to the gut of their new host. Dinospores were described in ''Haplozoon dogieli''. Sporomeres were observed detaching from adult trophonts and developing into small flagellated dinospores. They were 12 μm in length and similar to the dinospores of ''

Oodinium ''Oodinium'' is a genus of parasitic dinoflagellates. Their hosts are salt- and fresh-water fish, causing a type of fish velvet disease (also called gold dust disease). One species has also been recorded on various cnidarians. The host typica ...

'', ''Apodinium'', and ''Blastodinium''. These dinospores were also observed quickly encysting if disturbed. Subsequent studies have been unable to reproduce any dinospore or cyst life stages, and so no image data for these stages currently exists. While the existence of dinospores is likely, they have not been observed since 1924.

Phylogeny

Modern dinoflagellate phylogenies recognize 8 orders:

Syndiniales The Syndiniales are an order of early branching dinoflagellates (also known as Marine Alveolates, "MALVs"), found as parasites of crustaceans, fish, algae, cnidarians, and protists (ciliates, radiolarians, other dinoflagellates). The trophic ...

, Gymnodiniales,

Noctilucales The Noctilucales are an order of marine dinoflagellates. They differ from most others in that the mature cell is diploid and its nucleus does not show a dinokaryotic organization. They show gametic meiosis. Characteristics These cells are very ...

Suessiales Suessiales is an order of dinoflagellates. It includes '' Borghiella'', '' Glenodinium'', ''Polarella'' and ''Symbiodinium : ''This is about the genus sometimes called Zoox. For the company, see Zoox (company)'' ''Symbiodinium'' is a genus ...

, Peridiniales,

Gonyaulacales Gonyaulacales is an order of dinoflagellate The dinoflagellates (Greek δῖνος ''dinos'' "whirling" and Latin ''flagellum'' "whip, scourge") are a monophyletic group of single-celled eukaryotes constituting the phylum Dinoflagellata and are ...

Prorocentrales The Prorocentrales are a small order of dinoflagellates. They are distinguished by having their two flagella inserted apically, rather than ventrally as in other groups. One flagellum extends forward and the other circles its base, and there are ...

, and Dinophysiales. But this has not always been the case – early in the study of dinoflagellates, other orders were used such as Blastodiniales. Originally, Blastodiniales was a group for all parasitic dinoflagellates. Through the years, Blastodiniales has fallen out of favour and use. Subsequent phylogenetic analyses have confirmed that Blastodiniales is a

polyphyletic A polyphyletic group is an assemblage of organisms or other evolving elements that is of mixed evolutionary origin. The term is often applied to groups that share similar features known as homoplasies, which are explained as a result of conver ...

group, whose existence is not supported by modern molecular data. There is a history of former members of Blastodiniales being moved to new orders based on molecular data. As of June 2020, molecular data exists for five ''Haplozoon'' species: ''H. axiothellae, H. praxillellae, H. ezoense, H. gracile,'' and ''H. pugnus.''Yamamoto, Mana, et al. "Molecular phylogeny and ultrastructure of two novel parasitic dinoflagellates, ''Haplozoon gracile'' sp. nov. and ''H. pugnus'' sp. nov." ''Phycologia'' (2020): 1-15. Beyond being dinoflagellates, 18S phylogenetic analyses have failed to resolve the position of ''Haplozoon''. Therefore, ''Haplozoon'' remain in the polyphyletic order Blastodiniales, awaiting conclusive molecular data that confirms its true phylogenetic position. The following species are known to exist:Gómez, F. (2012). "A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata)." ''Cicimar Oceánides'', 27(1), 65-140. * '' H. armatum'', Dogiel, 1906 (host: ''Travisia forbesi'') * '' H. lineare'', Dogiel, 1907 (host: ''Clymene lumbricalis'') * '' H. delicatulum'', Dogiel, 1910 (Host: maldanid, gen sp?) * '' H. ariciae'', Dogiel, 1910 (host: ''Aricia norvegica'') * '' H. macrostylum'', Dogiel, 1910 (host: maldanid, gen sp?) * '' H. obscurum'', Dogiel, 1910 (host: ''Terebellides strömii'') * '' H. clymenellae'', Calkins, 1915 (host: ''Clymenella torquata'') * '' H. clymenidis'', Dogiel & Mikelsson, 1923 (host: ''Euclymene palermitana'') * '' H. tuberculatum'', Dogiel & Mikelsson 1923 (host: maldanid gen sp?) * '' H. villosum'', Dogiel & Mikelsson 1923 (host: ''Polyphysia crassa'', formerly ''Eumenia crassa'') * '' H. dogielii'', Shumway, 1924 (host: ''Leiochone clypeata'') * '' H. inerme'', Cachon 1964 (host: ''Appendicularia sicula'') * '' H. axiothellae'', Siebert, 1973 (host: ''Axiothellae rubrocincta'') * '' H. praxillellae'', Rueckert and Leander, 2008 (host: ''Praxillella pacifica'') * '' H. ezoense'', Wakeman, 2018 (host: ''Praxillella pacifica'') * '' H.gracile'' Yamamoto, 2020 (host: ''cf. Petaloclymene sp.'') * '' H.pugnus'' Yamamoto, 2020 (host: ''Nicomache personata, Nicomache sp.'')

References

{{Taxonbar, from=Q5892145 Dinophyceae Dinoflagellate genera