Sphaerospora molnari

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Sphaerospora molnari
S. molnari.jpg
Figure 1: Fresh spores of S. molnari in a gill smear of common carp (1; size bar 10 μm) and histological section of heavily infected gill filaments with spore-forming stages labelled in blue (2; size bar 100 μm); from Eszterbauer et al., 2013
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Cnidaria
Class: Myxosporea
Order: Bivalvulida
Family: Sphaerosporidae
Genus: Sphaerospora
Species:
S. molnari
Binomial name
Sphaerospora molnari
Lom, Dyková, Pavlásková and Grupcheva, 1983
Scanning electron microscopy image of proliferative S. molnari stages. The surface folds promote the motility of these stages in carp blood; size bar=1 mm; from Hartigan et al., 2016 Figure 2 S. molnari stages.jpg
Scanning electron microscopy image of proliferative S. molnari stages. The surface folds promote the motility of these stages in carp blood; size bar=1 μm; from Hartigan et al., 2016

Sphaerospora molnari is a microscopic endoparasite of carp ( Cyprinus carpio) in pond cultures and natural freshwater habitats in Central and Eastern Europe. [1] [2] In natural infections, S. molnari invades the epithelia of gills and surrounding skin regions. It then forms spores in between epithelial cells, [3] causing sphaerosporosis, [1] a pathological condition of the skin and gill tissues. Affected tissues show marked dystrophic changes and necrosis, [4] [5] [6] causing secondary bacterial infections and resulting in osmoregulatory and respiratory failure. Mortalities can reach 100% [6] but little is known about the overall distribution of the parasite species in European carp ponds or its economic impact on carp aquaculture.

Contents

Taxonomy

Before 1983, S. molnari was identified as S. carassii. Thereafter, it was distinguished from S. carassii (Kudo, 1919) and S. chinensis [1] based on spore morphology, host species and geographic locality. [1] Based on 18S rDNA sequences, S. molnari belongs to a well-defined taxonomic clade of myxozoans, Sphaerospora sensu stricto. [7] This clade of myxosporeans is composed mostly of endoparasites infecting the urinary system of marine and freshwater fish, and it is characterized by extremely large inserts in the 18S rDNA gene sequence, [8] [9] with S. molnari possessing the longest known myxozoan 18S rDNA sequence (3714 bp) and one of the longest amongst eukaryotes. [8] [10]

Life cycle

The life cycle for S. molnari has not yet been identified, but its closest relative, [9] [10] S. dykovae [1] was experimentally shown to cycle between an oligochaete worm as invertebrate host and common carp as vertebrate host. [11] The molecular identity of the two life cycle stages of S. dykovae is unconfirmed.

Pathology and clinical signs

S. molnari pathology involves inflammatory changes in the affected epithelia, accompanied by marked dystrophic changes and finally necrosis. [1] Necrotic disintegration of infected tissue results in the release of spores into the environment and transmission to the next host. Clinical signs are respiratory distress and pale gills. The early, presporogonic development of S. molnari includes parasite multiplication in the blood, [10] [12] likely a common cycle of development of the members of Sphaerospora sensu stricto. [8] Most recently, it has been demonstrated that this early development causes a massive inflammatory response with strongly increased lymphocyte numbers and likely a specific B cell response, and that partial immunity is acquired. [13] This may help to explain why the disease is associated with fry and fingerlings but not older carp. [1] [5]

Impact

The impact of gill and skin sphaerosporosis of common carp on carp aquaculture cannot presently be estimated but an increased occurrence of S. molnari proliferative blood stages in carp ponds in Czech Republic and Hungary was reported in 2014. A link to increasing pond temperatures due to climate change was proposed. [14]

Diagnosis

Proliferative blood stages are highly motile and can easily be differentiated from other blood parasites of common carp due to a unique motility mode. [12] Spores in the gills meet the characteristic diagnostic features of the genus Sphaerospora and are spherical spores with a spore length=spore width of approx. 10 μm and subspherical polar capsules measuring 4.7 (length) x 3.9 (width) μm. [1] [10] 18S rDNA sequences are available on GenBank under the accession numbers JX431511, JX431510, AF378345. Accession number AF378345 is likely an erroneous sequence. [10] The full ribosomal RNA sequence is available under accession number MK533682, a transcriptomic dataset from motile blood stages is published as Bioproject PRJNA522909 (SRX5386637). Specific PCR [10] and qPCR [13] assays exist and are able to differentiate the species from congeners occurring in the same host and quantify parasite numbers.[ citation needed ]

Treatments

There are presently no treatments against myxozoans in fish destined for human consumption. Ganeva et al. [15] demonstrated the effectiveness of certain in-feed treatments against S. molnari, with reduced parasite numbers in the blood of carp receiving diets enriched with certain parasiticidal and immunostimulatory substances.[ citation needed ]

Other control strategies

No other control strategies have been identified.

Research

Important limitations regarding in vivo models are a major reason for the limited information on host-parasite interactions in myxozoans and their hosts. Of more than 2600 known myxozoan species, only 55 life cycles have been elucidated to date, [16] and very few (3-4) are continuously perpetuated in research laboratories, as their maintenance is laborious and time-consuming, with the production of fish-infective spore stages in oligochaete or polychaete cultures spanning over several weeks or months. [17] One of the aims of the EU-funded Horizon 2020 Project ParaFishControl, was to establish the first in vivo and in vitro culture system for myxozoan proliferative stages (based on S. molnari blood stages), excluding full life cycle production. Such a system allows for the production of large numbers of host-free parasite stages for genomic/transcriptomic analyses, analyses on host-parasite interactions, and the establishment of test systems for antiparasitic/immunostimulatory substances, molecular interference approaches or vaccine trial. An experimental research model for proliferative stages is urgently required for myxozoans, for which no treatments are available but which appear to be an important group of fish parasites on the rise. First transcriptomic datasets of blood stages have been studied with regard to its arsenal of proteolytic enzymes, [18] which have demonstrated a great potential for vaccine design in other parasites.

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<span class="mw-page-title-main">Common carp</span> Species of fish

The common carp, also known as European carp or Eurasian carp, is a widespread freshwater fish of eutrophic waters in lakes and large rivers in Europe and Asia. The native wild populations are considered vulnerable to extinction by the International Union for Conservation of Nature (IUCN), but the species has also been domesticated and introduced into environments worldwide, and is often considered a destructive invasive species, being included in the list of the world's 100 worst invasive species. It gives its name to the carp family, Cyprinidae.

<span class="mw-page-title-main">Myxozoa</span> Subphylum of aquatic parasites

Myxozoa is a subphylum of aquatic cnidarian animals – all obligate parasites. It contains the smallest animals ever known to have lived. Over 2,180 species have been described and some estimates have suggested at least 30,000 undiscovered species. Many have a two-host lifecycle, involving a fish and an annelid worm or a bryozoan. The average size of a myxosporean spore usually ranges from 10 μm to 20 μm, whereas that of a malacosporean spore can be up to 2 mm. Myxozoans can live in both freshwater and marine habitats.

<span class="mw-page-title-main">Myxosporea</span> Class of cnidarians comprising microscopic parasites

Myxosporea is a class of microscopic animals, all of whom are parasites. They belong to the Myxozoa clade within Cnidaria. They have a complex life cycle that comprises vegetative forms in two hosts—one an aquatic invertebrate and the other an ectothermic vertebrate, usually a fish. Each parasitized host releases a different type of spore. The two forms of spore are so different that until relatively recently they were treated as belonging to different classes within the Myxozoa.

<i>Myxobolus cerebralis</i> Species of parasite

Myxobolus cerebralis is a myxosporean parasite of salmonids that causes whirling disease in farmed salmon and trout and also in wild fish populations. It was first described in rainbow trout in Germany in 1893, but its range has spread and it has appeared in most of Europe, the United States, South Africa, Canada and other countries from shipments of cultured and wild fish. In the 1980s, M. cerebralis was found to require a tubificid oligochaete to complete its life cycle. The parasite infects its hosts with its cells after piercing them with polar filaments ejected from nematocyst-like capsules. This infects the cartilage and possibly the nervous tissue of salmonids, causing a potentially lethal infection in which the host develops a black tail, spinal deformities, and possibly more deformities in the anterior part of the fish.

<i>Myxobolus</i> Genus of marine parasites

Myxobolus is a genus of myxozoa that includes important parasites of fish like Myxobolus cerebralis. The genus is polyphyletic, with members scattered throughout the myxozoa. Some stages of Myxobolus species were previously thought to be different organisms entirely, but are now united in this group. Some fish species, such as the thicklip grey mullet, can harbour a dozen of Myxobolus species.

<span class="mw-page-title-main">Myxobolidae</span> Family of marine parasites

Myxobolidae is a family of myxosporean parasites which typically infect freshwater fishes, and includes the economically significant species, Myxobolus cerebralis. They have been shown to have a complex life cycle, involving an alternate stage in an invertebrate, typically an annelid or polychaete worm.

Tetracapsuloides bryosalmonae is a myxozoan parasite of salmonid fish. It is the only species currently recognized in the monotypic genus Tetracapsuloides. It is the cause of proliferative kidney disease (PKD), one of the most serious parasitic diseases of salmonid populations in Europe and North America that can result in losses of up to 90% in infected populations.

Kudoa thyrsites is a myxosporean parasite of marine fishes. It has a worldwide distribution, and infects a wide range of host species. This parasite is responsible for causing economic losses to the fisheries sector, by causing post-mortem "myoliquefaction", a softening of the flesh to such an extent that the fish becomes unmarketable. It is not infective to humans.

<span class="mw-page-title-main">Xenoma</span> Growth caused by various species of protists and fungi

A xenoma is a growth caused by various protists and fungi, most notably microsporidia. It can occur on numerous organisms; however is predominantly found on fish.

<i>Henneguya zschokkei</i> Species of Myxosporea

Henneguya zschokkei or Henneguya salminicola is a species of a myxosporean endoparasite. It afflicts several salmon in the genera Oncorhynchus and Salmo,where it causes milky flesh or tapioca disease. H. zschokkei is notable for its reliance on an exclusively anaerobic metabolism as well as its lack of mitochondria and mitochondrial DNA. It is the only known multicellular animal that does not require oxygen to survive.

Goussia is a taxonomic genus, first described in 1896 by Labbé, containing parasitic protists which largely target fish and amphibians as their hosts. Members of this genus are homoxenous and often reside in the gastrointestinal tract of the host, however others may be found in organs such as the gallbladder or liver. The genera Goussia, as current phylogenies indicate, is part of the class Conoidasida, which is a subset of the parasitic phylum Apicomplexa; features of this phylum, such as a distinct apical complex containing specialized secretory organelles, an apical polar ring, and a conoid are all present within Goussia, and assist in the mechanical invasion of host tissue. The name Goussia is derived from the French word gousse, meaning pod. This name is based on the bi-valve sporocyst morphology which some Goussians display. Of the original 8 classified Goussians, 6 fit the “pod” morphology. As of this writing, the genera consists of 59 individual species.

<i>Kudoa</i> Genus of marine parasites

Kudoa is a genus of Myxozoa and the only genus recognized within the monotypic family Kudoidae. There are approximately 100 species of Kudoa all of which parasitize on marine and estuarine fish. Kudoa are most commonly known and studied for the negative effects the genus has on commercial fishing and aquaculture industries.

Gadimyxa atlantica is a species of parasitic myxozoan. Together with G. arctica and G. sphaerica, they infect Gadus morhua and Arctogadus glacialis by developing coelozoically in bisporic plasmodia in their urinary systems. These 3 species' spores exhibit two morphological forms: wide and subspherical, being both types bilaterally symmetrical along the suture line. The wide spores have a mean width ranging from 7.5-10μm, respectively, while the subspherical ones range from 5.3-8μm in mean width. The subspherical forms of Gadimyxa are similar to Ortholinea, differing in the development of the spores and in the arrangement of the polar capsules. Polychaetes Spirorbisspecies act as invertebrate hosts of G. atlantica.

Gadimyxa sphaerica is a species of parasitic myxozoan. Together with G. arctica and G. atlantica, they infect Gadus morhua and Arctogadus glacialis by developing coelozoically in bisporic plasmodia in their urinary systems. These 3 species' spores exhibit two morphological forms: wide and subspherical, being both types bilaterally symmetrical along the suture line. The wide spores have a mean width ranging from 7.5 to 10μm, respectively, while the subspherical ones range from 5.3-8μm in mean width. The subspherical forms of Gadimyxa are similar to Ortholinea, differing in the development of the spores and in the arrangement of the polar capsules.

Gadimyxa arctica is a species of parasitic myxozoan. Together with G. atlantica and G. sphaerica, they infect Gadus morhua and Arctogadus glacialis by developing coelozoically in bisporic plasmodia in their urinary systems. These 3 species' spores exhibit two morphological forms: wide and subspherical, being both types bilaterally symmetrical along the suture line. The wide spores have a mean width ranging from 7.5-10μm, respectively, while the subspherical ones range from 5.3-8μm in mean width. The subspherical forms of Gadimyxa are similar to Ortholinea, differing in the development of the spores and in the arrangement of the polar capsules.

Saccosporidae is a family of myxozoans. It is the only family within the class Malacosporea and has only three species, while the other class of Myxozoa, Myxosporea, includes more than a thousand.

<i>Enteromyxum leei</i> Species of marine parasite

Enteromyxum leei is a species of myxozoan, histozoic parasite that infects the intestinal tract and sometimes associated organs, like gall bladder and liver, of several teleostean fish species. Myxozoans are microscopic metazoans, with an obligate parasitic life-style. The parasite stages of this species live in the paracelullar space between fish enterocytes. It is the causative agent of enteromyxosis, or emaciative disease, also known as "razor blade syndrome" in sparid fish. E. leei has a wide host and geographical range within marine fish, and even freshwater fish have been infected experimentally. E. leei initially emerged in the Mediterranean in the late 1980s and it is believed to have been unintentionally introduced into the Red Sea. Its pathogenicity and economic impact depend on the host species. In the gilt-head seabream, it is manifested as a chronic disease that provokes anorexia, delayed growth with weight loss, cachexia, reduced marketability and increased mortality. In other species, it has no clinical signs. In sharpsnout seabream, infection results in very high mortality rates, which have pushed fish farmers to abandon the culture of this fish species.

<i>Thelohanellus kitauei</i> Parasite of carp

Thelohanellus kitauei is a myxozoan endoparasite identified as the agent of intestinal giant-cystic disease (IGCD) of common carp Cyprinus carpio. The species was first identified in Japan, in 1980 and later formally described by Egusa & Nakajima. Fan subsequently reported the parasite in China, and several other reports from carp and Koi carp in China and Korea followed. Reports referred to an intestinal infection, swelling and emaciation of fish due to blockage of the intestinal tract by giant cysts. The intestine of carp was believed to be the only infection site of T. kitauei until Zhai et al. reported large cysts of T. kitauei in the skin, with morphologically similar and molecularly identical spores. T. kitauei has been recognized as the most detrimental disease of farmed carp in Asia with around 20% of farmed carp killed annually. In 2014, the genome of T. kitauei was sequenced, and in 2016, its life cycle was found to include the oligochaete Branchiura sowerbyi. Infected oligochaete worms were first discovered in Hungary and raised concerns of the introduction of T. kitauei into European carp culture ponds, since it was believed to be endemic to Asia. However, the related disease (IGCD) has not yet been reported in Europe.

<i>Myxidium</i> Genus of marine invertebrates

Myxidium is a genus of cnidarians belonging to the family Myxidiidae.

Zschokkella are identified as parasitic organisms from the family Myxidiidae of the suborder Variisporina. This genus of Myxozoa tend to inhabit common areas of their host and can be found around the globe in both marine to freshwater habitats. Zschokkella also have spore shapes and host specific parasitism that differentiates it from other Myxidiidae.

References

  1. 1 2 3 4 5 6 7 8 Lom J, Dyková I, Pavlásková M, Grupcheva G (1983). "Sphaerospora molnari sp. nov. (Myxozoa: Myxosporea), an agent of gill, skin and blood sphaerosporosis of common carp in Europe". Parasitology. 86 (3): 529–535. doi:10.1017/S003118200005071X.
  2. ↑ Dyková I, Lom J (1988). "Review of pathogenic myxosporeans in intensive culture of carp (Cyprinus carpio) in Europe". Folia Parasitologica. 35 (4): 289–307. ISSN   1803-6465 . Retrieved 27 November 2024.
  3. ↑ Kaup FJ, Kuhn EM, Körting W (1995) Light and electron microscopic studies on the sporogenesis of Sphaerospora molnari in the gill lamellas of carp (Cyprinus carpio). Berliner und Münchner Tierärztliche Wochenschrift 108: 206-214.
  4. ↑ Iskov MP (1969) Sphaerosporosis as a new disease of carp. Problemy parazitologii, Proceedings of the VIth Scientific Conference of Parasitology, Ukrainian SSR II, Naukova Dumka, Kiev, p 228−232
  5. 1 2 Molnár K (1977) Gill sphaerosporosis in the common carp and grasscarp. Acta Veterinaria Academiae Scientiarum Hungaricae 27: 99−113.
  6. 1 2 Waluga D (1983) Preliminary investigations on carp sphaerosporosis. Medycyna Veterynaryjna 39: 399−403.
  7. ↑ Jirku M, Fiala I, Modrý D (2007) Tracing the genus Sphaero spora: rediscovery, redescription and phylogeny of Sphaerospora ranae (Morelle, 1929) n. comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology 134: 1727−1739.
  8. 1 2 3 Bartošová P, Fiala I, Jirků M, Cinková M, Caffara M, Fioravanti ML, et al. (2013) Sphaerospora sensu stricto: Taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Molecular Phylogenetics and Evolution 68:93–105.
  9. 1 2 Patra S, Bartošová-Sojková P, Pecková H, Fiala I, Eszterbauer E, Holzer AS (2018) Biodiversity and host-parasite cophylogeny of Sphaerospora (sensu stricto) (Cnidaria: Myxozoa). Parasites & Vectors 11:347.
  10. 1 2 3 4 5 6 Eszterbauer E, Sipos D, Forró B, Bartošová P, Holzer A. (2013) Molecular characterization of Sphaerospora molnari (Myxozoa), the agent of gill sphaerosporosis in common carp Cyprinus carpio. Diseases of Aquatic Organisms 104: 59–67.
  11. ↑ Molnár K, El-Mansy A, Székely C, Baska F (1999). "Experimental identification of the actinosporean stage of Sphaerospora renicola Dyková & Lom, 1982 (Myxosporea: Sphaerosporidae) in oligochaete alternate hosts". Journal of Fish Diseases. 22 (2): 143–153. doi:10.1046/j.1365-2761.1999.00150.x.
  12. 1 2 Hartigan A, Estensoro I, Vancová M, Bílý T, Patra S, Eszterbauer E, Holzer AS (2016). "New cell motility model observed in parasitic cnidarian Sphaerospora molnari (Myxozoa:Myxosporea) blood stages in fish". Scientific Reports. 6. doi: 10.1038/srep39093 . Art. No. 39093.
  13. 1 2 Korytar T, Wiegertjes G, Zuskova E, Tonanova A, Lisnerova M, Patra S, Sieranski V, Sima R, Born-Torrijos A, Wentzel AS, Blasco-Monleon S, Yanes-Roca C, Policar T, Holzer AS (2019). The kinetics of cellular and humoral immune responses of common carp to presporogonic development of the myxozoan Sphaerosporamolnari. Parasites & Vectors 12:208. doi: https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-019-3462-3
  14. ↑ Holzer AS, Hartigan A, Patra S, Pecková H, Eszterbauer E (2014) Molecular fingerprinting of the myxozoan community in common carp suffering Swim Bladder Inflammation (SBI) identifies multiple etiological agents. Parasites & Vectors 7:398.
  15. ↑ Ganeva V, Korytář T, Mullins J, McGurk C, Holzer AS (2018) impact of in-feed treatments on common carp immune system in response to infection with Sphaerospora molnari (Myxozoa:Cnidaria). Poster presented at the 14th ISDCI Congress, Santa Fe, New Mexico, 17th-21st June 2018.
  16. ↑ Holzer AS, Bartošová-Sojková P, Born-Torrijos A, Lövy A, Hartigan A, Fiala I (2018) The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity. Molecular Ecology 27: 1651-1666.
  17. ↑ Eszterbauer E, Atkinson S, Diamant A, Morris D, El-Matbouli M, Hartikainen H (2015) Myxozoan live cycles: practical approaches and insights. In: Myxozoan Evolution, Ecology and Development. B. Okamura et al. (Eds.): pp.139-154.
  18. ↑ Hartigan A, Kosakyan A, Pecková H, Eszterbauer E, Holzer AS (2020) Transcriptome of Sphaerospora molnari(Cnidaria, Myxosporea) blood stages provides proteolytic arsenal as potential therapeutic targets against sphaerosporosis in common carp. BMC Genomics in press.
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