Philasterides dicentrarchi

Last updated

Philasterides dicentrarchi
Scientific classification
Domain:
Eukaryota
(unranked):
SAR
(unranked):
Alveolata
Phylum:
Ciliophora
Class:
Oligohymenophorea
Subclass:
Scuticociliatia
Order:
Philasterida
Family:
Philasteridae
Genus:
Philasterides
Species:
Philasterides dicentrarchi
Figure 1: "Philasterides dicentrarchi, image provided by Jose Manuel Leiro, Jesus Lamas. University of Santiago de Compostela" Philasterides dicentrarchi.png
Figure 1: “Philasterides dicentrarchi, image provided by José Manuel Leiro, Jesús Lamas. University of Santiago de Compostela”

Philasterides dicentrarchi is a marine protozoan ciliate that was first identified in 1995 after being isolated from infected European sea bass (Dicentrarchus labrax) reared in France. [1] The species was also identified as the causative agent of outbreaks of scuticociliatosis that occurred between summer 1999 and spring 2000 in turbot (Scophthalmus maximus) cultivated in the Atlantic Ocean (Galicia, Northwest Spain). [2] Infections caused by P. dicentrarchi have since been observed in turbot reared in both open flow and recirculating production systems. [3] In addition, the ciliate has also been reported to cause infections in other flatfishes, such as the olive flounder (Paralichthys olivaceus) in Korea [4] and the fine flounder (Paralichthys adspersus) in Peru, [5] as well as in seadragons ( Phyllopteryx taeniolatus and Phycodurus eques ), [6] [7] seahorses (Hippocampuskuda and H. abdominalis ), [8] and several species of sharks [9] in other parts of the world.

Contents

Biology and pathology

P. dicentrarchi is included within the subclass Scuticociliatia, which includes about 20 species of ciliates that are typically microphagous bacteriovores and generally abundant in eutrophic habitats in lakes and in coastal marine habitats. Some of these ciliates, characterized by possessing a scutica (a transient kinetosomal structure that is present during stomatogenesis), can behave as endoparasites and are capable of producing serious infections in a wide variety of vertebrates, especially fish, and invertebrates such as crustaceans and echinoderms. [4] [10] [11] [12] [13] [14] P. dicentrarchi is a microaerophilic scuticociliate that lives at the sea bottom, at or below the oxycline or on the monimolimnion, where it feeds on bacteria. [15] However, when it encounters a host it can also behave as an opportunistic histiophagous parasite. [2] Survival of the species inside the host and adaptation to a parasitic lifestyle are attributed to the existence of physiological adaptations at the level of mitochondrial metabolism. Such adaptations include the presence of a second terminal oxidase (which enables the ciliates to obtain energy and survive low levels of oxygen [16] ), antioxidant enzymes, [17] inorganic pyrophosphatases (capable of producing energy by an ATP alternative pathway produced during oxidative metabolism) and the ability of the species to survive in hyposaline environments. [18] Although the route of entry to the host is unknown, the findings of experimental infection studies suggest that the ciliate probably gains access through lesions in the gills and/or the skin. [19] Infected fish show haemorrhagic ulcers on the skin (particularly around the operculum), abundant ascitic fluid in the abdominal cavity, uni- or bilateral exophthalmia, and systemic infection with the presence of ciliates in blood, gills, gastrointestinal tract, liver, spleen, kidneys and musculature. In the final phase of infection, ciliates reach the brain and cause softening and liquefaction of the tissue. [2]

Diagnosis

Diagnosis of P. dicentrarchi in the sea bass and the turbot was initially based primarily on morphological characteristics associated with the oral apparatus and the number of kineties. [1] [2] However, it has been suggested that the combined use of morphological, biological, molecular and serological techniques is necessary for correct identification of the species. [3] [6] P. dicentrarchi was previously considered a junior synonym of Miamiensis avidus . [20] However, recent physiological and molecular studies have shown that P. dicentrarchi and M. avidus strain Ma/2 -ATCC 50180™- are different species. [5]

Treatments

No effective chemotherapeutic measures have been developed for controlling scuticociliatosis in the acute phase of the disease to date. However, the addition of disinfectants such as formalin, hydrogen peroxide and Jenoclean (a mixture of Atacama extract 97%-Zeolites- and citric acid 3%) to seawater has been demonstrated to kill the ciliates. [12] [21] [22] Bath treatments consisting of a combination of benzalkonium chloride and bronopol have also proved to be effective in reducing fish mortality. [23] Several compounds of well-known antiprotozoal activity, including niclosamide, oxyclozanide, bithionol sulfoxide, toltrazuril, N-(2 '-hydroxy-5 '-chloro-benzoyl) 2-chloro-4-nitroaniline, BP68, doxycycline hyclate, albendazole, carnidazole, pyrimethamine, hydrochloride quinacrine and quinine sulphate, are also active against P. dicentrarchi. [21] Antimalarial drugs such as chloroquine and artemisinin also inhibit the in vitro growth of P. dicentrarchi. [24] Other studies investigating the in vitro effects of several new synthetic compounds, including 2 naphthyridines, 2 pyridothienodiazines and 13 pyridothienotriazines, have demonstrated that all display parasiticide activity, and that pyridothienotriazine (12k) was the most active. [25] In addition, several compounds of natural origin have also shown in vitro antiparasitic activity: the polyphenols mangiferin and (–)-epigallocatechin-3-gallate (EGCG), [26] curcumin, [27] resveratrol [28] and the synthetic polyphenol propyl gallate. [29]

Prevention

Vaccines containing trophozoites inactivated with formalin and prepared in oil adjuvants have been developed and have shown good protection against the homologous serotype. [30] [31] Several P. dicentrarchi serotypes have been described. However, the protection induced against heterologous isolates appears to be very low or non-existent. [32]

Research

Research on Philasterides dicentrarchi, which includes aspects of cell biology, diagnostics, interactions with the host immune system, search for new treatments, development of vaccines or risk analysis, is being carried out under the EU funded Horizon2020 Project ParaFishControl. [33]

Related Research Articles

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Ichthyophthirius multifiliis, often termed "Ich", is a parasitic ciliate described by the French parasitologist Fouquet in 1876. Only one species is found in the genus which also gave name to the family. The name literally translates as "the fish louse with many children". The parasite can infect most freshwater fish species and, in contrast to many other parasites, shows low host specificity. It penetrates gill epithelia, skin and fins of the fish host and resides as a feeding stage inside the epidermis. It is visible as a white spot on the surface of the fish but, due to its internal microhabitat, it is a true endoparasite and not an ectoparasite.

<span class="mw-page-title-main">Parasitic disease</span> Medical condition

A parasitic disease, also known as parasitosis, is an infectious disease caused by parasites. Parasites are organisms which derive sustenance from its host while causing it harm. The study of parasites and parasitic diseases is known as parasitology. Medical parasitology is concerned with three major groups of parasites: parasitic protozoa, helminths, and parasitic arthropods. Parasitic diseases are thus considered those diseases that are caused by pathogens belonging taxonomically to either the animal kingdom, or the protozoan kingdom.

<i>Balantidium</i> Genus of single-celled organisms

Balantidium is a genus of ciliates. It contains the parasitic species Balantidium coli, the only known cause of balantidiasis.

<i>Echinostoma</i> Genus of flukes

Echinostoma is a genus of trematodes (flukes), which can infect both humans and other animals. These intestinal flukes have a three-host life cycle with snails or other aquatic organisms as intermediate hosts, and a variety of animals, including humans, as their definitive hosts.

<span class="mw-page-title-main">Sea louse</span> Family of copepods

Sea lice are copepods of the family Caligidae within the order Siphonostomatoida. They are marine ectoparasites that feed on the mucus, epidermal tissue, and blood of host fish. The roughly 559 species in 37 genera include around 162 Lepeophtheirus and 268 Caligus species.

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

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<i>Cryptocaryon</i> Genus of single-celled organisms

Cryptocaryon irritans is a species of ciliates that parasitizes marine fish, causing marine white spot disease or marine ich. It is one of the most common causes of disease in marine aquaria.

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<span class="mw-page-title-main">Mobilida</span> Order of protists belonging to the ciliates phylum

Mobilida is a group of parasitic or symbiotic peritrich ciliates, comprising more than 280 species. Mobilids live on or within a wide variety of aquatic organisms, including fish, amphibians, molluscs, cnidarians, flatworms and other ciliates, attaching to their host organism by means of an aboral adhesive disk. Some mobilid species are pathogens of wild or farmed fish, causing severe and economically damaging diseases such as trichodinosis.

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Tenacibaculum is a Gram-negative and motile bacterial genus from the family of Flavobacteriaceae.

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<span class="mw-page-title-main">Philasterida</span> Order of single-celled organisms

Philasterida is an order of ciliates in the subclass Scuticociliatia.

Miamiensis avidus is a species of unicellular marine eukaryote that is a parasite of many different types of fish. It is one of several organisms known to cause the fish disease scuticociliatosis and is considered an economically significant pathogen of farmed fish. M. avidus is believed to be the cause of a 2017 die-off of fish and sharks in the San Francisco Bay.

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

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Philasterides is a genus of ciliates in the order Philasteridae.

References

  1. 1 2 Dragesco, Armelle; Dragesco, Jean; Coste, Françoise; Gasc, Charles; Romestand, Bernard; Raymond, Jean-Christophe; Bouix, Georges (1995). "Philasterides dicentrarchi, n. Sp., (Ciliophora, scuticociliatida), a histophagous opportunistic parasite of Dicentrarchus labrax (Linnaeus, 1758), a reared marine fish". European Journal of Protistology. 31 (3): 327–340. doi:10.1016/S0932-4739(11)80097-0.
  2. 1 2 3 4 Iglesias, R.; Paramá, A.; Alvarez, MF; Leiro, J.; Fernández, J.; Sanmartín, ML (2001). "Philasterides dicentrarchi (Ciliophora, Scuticociliatida) as the causative agent of scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain)". Diseases of Aquatic Organisms. 46 (1): 47–55. doi: 10.3354/dao046047 . PMID   11592702.
  3. 1 2 Budiño, Belén; Lamas, Jesús; Pata, María P.; Arranz, Juan A.; Sanmartín, Manuel L.; Leiro, José (2011). "Intraspecific variability in several isolates of Philasterides dicentrarchi (Syn. Miamiensis avidus), a scuticociliate parasite of farmed turbot". Veterinary Parasitology. 175 (3–4): 260–272. doi:10.1016/j.vetpar.2010.10.011. PMID   21036479.
  4. 1 2 Kim, SM; Cho, JB; Kim, SK; Nam, YK; Kim, KH (2004). "Occurrence of scuticociliatosis in olive flounder Paralichthys olivaceus by Phiasterides dicentrarchi (Ciliophora: Scuticociliatida)". Diseases of Aquatic Organisms. 62 (3): 233–238. doi: 10.3354/dao062233 . PMID   15672879.
  5. 1 2 De Felipe, ANA-Paula; Lamas, Jesús; Sueiro, Rosa-ANA; Folgueira, Iria; Leiro, José-Manuel (2017). "New data on flatfish scuticociliatosis reveal that Miamiensis avidus and Philasterides dicentrarchi are different species". Parasitology. 144 (10): 1394–1411. doi:10.1017/S0031182017000749. hdl: 10261/177213 . PMID   28552088. S2CID   7694270.
  6. 1 2 Umehara, Azusa; Kosuga, Yuko; Hirose, Hitomi (2003). "Scuticociliata infection in the weedy sea dragon Phyllopteryx taeniolatus". Parasitology International. 52 (2): 165–168. doi:10.1016/S1383-5769(02)00080-6. PMID   12798928.
  7. ↑ Rossteuscher, S.; Wenker, C.; Jermann, T.; Wahli, T.; Oldenberg, E.; Schmidt-Posthaus, H. (2008). "Severe Scuticociliate (Philasterides dicentrarchi) Infection in a Population of Sea Dragons (Phycodurus eques and Phyllopteryx taeniolatus)". Veterinary Pathology. 45 (4): 546–550. doi: 10.1354/vp.45-4-546 . PMID   18587104.
  8. ↑ Di Cicco, Emiliano; Paradis, Erika; Stephen, Craig; Turba, Maria Elena; Rossi, Giacomo (2013). "Scuticociliatid Ciliate Outbreak in Australian Pot-Bellied Seahorse,hippocampus Abdominalis(Lesson, 1827): Clinical Signs, Histopathologic Findings, and Treatment with Metronidazole". Journal of Zoo and Wildlife Medicine. 44 (2): 435–440. doi:10.1638/2012-127R1.1. PMID   23805562. S2CID   3167897.
  9. ↑ Stidworthy, M. F.; Garner, M. M.; Bradway, D. S.; Westfall, B. D.; Joseph, B.; Repetto, S.; Guglielmi, E.; Schmidt-Posthaus, H.; Thornton, S. M. (2014). "Systemic Scuticociliatosis (Philasterides dicentrarchi) in Sharks". Veterinary Pathology. 51 (3): 628–632. doi: 10.1177/0300985813492800 . PMID   23774745.
  10. ↑ Alvarez-Pellitero, Pilar; Palenzuela, Oswaldo; Padros, Francesc; Sitja-Bobadilla, Ariadna; Riaza, Ana; Silva, Raquel; Aran, Javier (2004). "Histophagous scuticociliatids (Ciliophora) parasitizing turbot Scophthalmus maximus: Morphology, in vitro culture and virulence". Folia Parasitologica. 51 (2–3): 177–187. doi: 10.14411/fp.2004.021 . hdl: 10261/20883 . PMID   15357395.
  11. ↑ Smith, PJ; McVeagh, SM; Hulston, D.; Anderson, SA; Gublin, Y. (2009). "DNA identification of ciliates associated with disease outbreaks in a New Zealand marine fish hatchery". Diseases of Aquatic Organisms. 86 (2): 163–167. doi: 10.3354/dao02113 . PMID   19902845.
  12. 1 2 Harikrishnan, Ramasamy; Jin, Chang-Nam; Kim, Man-Chul; Kim, Ju-Sang; Balasundaram, Chellam; Heo, Moon-Soo (2010). "Effectiveness and immunomodulation of chemotherapeutants against scuticociliate Philasterides dicentrarchi in olive flounder". Experimental Parasitology. 124 (3): 306–314. doi:10.1016/j.exppara.2009.11.005. PMID   19944688.
  13. ↑ Fan, Xinpeng; Hu, Xiaozhong; Al-Farraj, Saleh A.; Clamp, John C.; Song, Weibo (2011). "Morphological description of three marine ciliates (Ciliophora, Scuticociliatia), with establishment of a new genus and two new species". European Journal of Protistology. 47 (3): 186–196. doi:10.1016/j.ejop.2011.04.001. PMID   21570267.
  14. ↑ Pan, X.; Zhu, M.; Ma, H.; Al-Rasheid, K. A. S.; Hu, X. (2013). "Morphology and small-subunit rRNA gene sequences of two novel marine ciliates, Metanophrys orientalis spec. Nov. And Uronemella sinensis spec. Nov. (Protista, Ciliophora, Scuticociliatia), with an improved diagnosis of the genus Uronemella". International Journal of Systematic and Evolutionary Microbiology. 63 (Pt 9): 3515–3523. doi:10.1099/ijs.0.053173-0. PMID   23859947.
  15. ↑ Shimeta, J.; Sisson, JD (1999). "Taxon-specific tidal resuspension of protists into the subtidal benthic boundary layer of a coastal embayment". Marine Ecology Progress Series. 177: 51–62. Bibcode:1999MEPS..177...51S. doi: 10.3354/meps177051 .
  16. ↑ Mallo, Natalia; Lamas, Jesús; Leiro, José Manuel (2013). "Evidence of an Alternative Oxidase Pathway for Mitochondrial Respiration in the Scuticociliate Philasterides dicentrarchi". Protist. 164 (6): 824–836. doi:10.1016/j.protis.2013.09.003. PMID   24211656.
  17. ↑ Lamas, J.; Morais, P.; Arranz, J.A.; Sanmartín, M.L.; Orallo, F.; Leiro, J. (2009). "Resveratrol promotes an inhibitory effect on the turbot scuticociliate parasite Philasterides dicentrarchi by mechanisms related to cellular detoxification". Veterinary Parasitology. 161 (3–4): 307–315. doi:10.1016/j.vetpar.2008.12.025. PMID   19246159.
  18. ↑ Mallo, Natalia; Lamas, Jesús; Piazzon, Carla; Leiro, José M. (2015). "Presence of a plant-like proton-translocating pyrophosphatase in a scuticociliate parasite and its role as a possible drug target". Parasitology. 142 (3): 449–462. doi:10.1017/S0031182014001267. PMID   25118804. S2CID   1838881.
  19. ↑ Paramá, A.; Iglesias, R.; Álvarez, M.F; Leiro, J.; Aja, C.; Sanmartı́n, M.L (2003). "Philasterides dicentrarchi (Ciliophora, Scuticociliatida): Experimental infection and possible routes of entry in farmed turbot (Scophthalmus maximus)". Aquaculture. 217 (1–4): 73–80. doi:10.1016/S0044-8486(02)00523-9.
  20. ↑ Jung, SJ; Kitamura, SI; Song, JY; Oh, MJ (2007). "Miamiensis avidus (Ciliophora: Scuticociliatida) causes systemic infection of olive flounder Paralichthys olivaceus and is a senior synonym of Philasterides dicentrarchi". Diseases of Aquatic Organisms. 73 (3): 227–234. doi: 10.3354/dao073227 . PMID   17330742.
  21. 1 2 Iglesias, R.; Paramá, A.; Álvarez, MF; Leiro, J.; Sanmartín, ML (2002). "Antiprotozoals effective in vitro against the scuticociliate fish pathogen Philasterides dicentrarchi". Diseases of Aquatic Organisms. 49 (3): 191–197. doi: 10.3354/dao049191 . PMID   12113305.
  22. ↑ Budiño, B.; Pata, M. P.; Leiro, J.; Lamas, J. (2012). "Differences in the in vitro susceptibility to resveratrol and other chemical compounds among several Philasterides dicentrarchi isolates from turbot". Parasitology Research. 110 (4): 1573–1578. doi:10.1007/s00436-011-2664-1. PMID   21987103. S2CID   2160120.
  23. ↑ Park, Seong Bin; Jang, Ho Bin; Fagutao, Fernand F.; Kim, Young Kyu; Nho, Seong Won; Cha, In Seok; Yu, Jong Earn; Jung, Tae Sung (2014). "Combination treatment against scuticociliatosis by reducing the inhibitor effect of mucus in olive flounder, Paralichthys olivaceus". Fish & Shellfish Immunology. 38 (2): 282–286. doi:10.1016/j.fsi.2014.03.023. PMID   24704417.
  24. ↑ Mallo, Natalia; Lamas, Jesús; De Felipe, Ana-Paula; Sueiro, Rosa-Ana; Fontenla, Francisco; Leiro, José-Manuel (2016). "Role of H+-pyrophosphatase activity in the regulation of intracellular pH in a scuticociliate parasite of turbot: Physiological effects". Experimental Parasitology. 169: 59–68. doi:10.1016/j.exppara.2016.07.012. hdl: 10347/18174 . PMID   27480055.
  25. ↑ Paramá, A.; Iglesias, R.; Álvarez, F.; Leiro, JM; Quintela, JM; Peinador, C.; González, L.; Riguera, R.; Sanmartín, ML (2004). "In vitro efficacy of new antiprotozoals against Philasterides dicentrarchi (Ciliophora, Scuticociliatida)". Diseases of Aquatic Organisms. 62 (1–2): 97–102. doi: 10.3354/dao062097 . PMID   15648836.
  26. ↑ Leiro, J.; Arranz, JA; Paramá, A.; Álvarez, MF; Sanmartín, ML (2004). "In vitro effects of the polyphenols resveratrol, mangiferin and (–)-epigallocatechin-3-gallate on the scuticociliate fish pathogen Philasterides dicentrarchi". Diseases of Aquatic Organisms. 59 (2): 171–174. doi: 10.3354/dao059171 . PMID   15212284.
  27. ↑ Mallo, N.; Defelipe, A. P.; Folgueira, I.; Sueiro, R. A.; Lamas, J.; Leiro, J. M. (2017). "Combined antiparasitic and anti-inflammatory effects of the natural polyphenol curcumin on turbot scuticociliatosis". Journal of Fish Diseases. 40 (2): 205–217. doi:10.1111/jfd.12503. hdl: 10347/18168 . PMID   27334368.
  28. ↑ Morais, Pedro; Piazzon, Carla; Lamas, Jesús; Mallo, Natalia; Leiro, José M. (2013). "Effect of Resveratrol on Oxygen Consumption by Philasterides dicentrarchi, a Scuticociliate Parasite of Turbot". Protist. 164 (2): 206–217. doi:10.1016/j.protis.2012.07.002. PMID   22951214.
  29. ↑ Mallo, Natalia; Lamas, Jesús; Leiro, José M. (2014). "Alternative oxidase inhibitors as antiparasitic agents against scuticociliatosis". Parasitology. 141 (10): 1311–1321. doi:10.1017/S0031182014000572. PMID   24824550. S2CID   25367919.
  30. ↑ Sanmartín, M. L.; Paramá, A.; Castro, R.; Cabaleiro, S.; Leiro, J.; Lamas, J.; Barja, J. L. (2008). "Vaccination of turbot, Psetta maxima (L.), against the protozoan parasite Philasterides dicentrarchi: Effects on antibody production and protection". Journal of Fish Diseases. 31 (2): 135–140. doi:10.1111/j.1365-2761.2007.00876.x. PMID   18234021.
  31. ↑ Lamas, Jesús; Sanmartín, Manuel L.; Paramá, Ana I.; Castro, Rosario; Cabaleiro, Santiago; Ruiz De Ocenda, María V.; Barja, Juan L.; Leiro, José (2008). "Optimization of an inactivated vaccine against a scuticociliate parasite of turbot: Effect of antigen, formalin and adjuvant concentration on antibody response and protection against the pathogen". Aquaculture. 278 (1–4): 22–26. doi:10.1016/j.aquaculture.2008.03.015.
  32. ↑ Piazzón, C.; Lamas, J.; Castro, R.; Budiño, B.; Cabaleiro, S.; Sanmartín, M.; Leiro, J. (2008). "Antigenic and cross-protection studies on two turbot scuticociliate isolates". Fish & Shellfish Immunology. 25 (4): 417–424. doi:10.1016/j.fsi.2008.05.012. PMID   18602012.
  33. ↑ "Home". parafishcontrol.eu.
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