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Philasterides dicentrarchi

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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
Philasterides dicentrarchi
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 (Hippocampus kuda and H. abdominalis),[8] and several species of sharks[9] in other parts of the world.

Biology and pathology

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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

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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

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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

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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

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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]

References

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  1. ^ a b 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. ^ a b c d 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. ^ a b 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. ^ a b 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. ^ a b 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. ^ a b 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. ^ a b 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. Bibcode:2003Aquac.217...73P. 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. ^ a b 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. Bibcode:2014FSI....38..282P. 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. Bibcode:2017JFDis..40..205M. 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. Bibcode:2008JFDis..31..135S. 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. Bibcode:2008Aquac.278...22L. 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. Bibcode:2008FSI....25..417P. doi:10.1016/j.fsi.2008.05.012. PMID 18602012.
  33. ^ "Home". parafishcontrol.eu.
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