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Ciliate Uronema marinum is the causative agent of scuticociliatosis in farm raised turbot Scophthalmus maximus

  • Aquaculture and Fisheries
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Abstract

To identify the pathogen that causes scuticociliatosis in farmed-raised turbot Scophthalmus maximus, we isolated a ciliate from the brain tissue of an infected turbot and identified it as Uronema marinum based on morphological and molecular evidence. We then infected the turbots in artificial laboratory settings with pure cultured U. marinum. The infected turbots showed syndromes similar to those observed in naturally infected ones. Furthermore, microscopic examination and PCR detection confirmed the presence of the ciliate in the tissues of those laboratory-infected turbots. To our best knowledge, this is the first report of scuticociliatosis caused by U. marinum in farm-raised turbot S. maximus in China.

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References

  • Anderson S A, Hulston D A, McVeagh S M, Webb V L, Smith P J. 2009. In vitro culture and cryopreservation of Uronema marinum isolated from farmed New Zealand groper (Polyprion oxygeneios). Journal of Microbiological Methods, 79(1): 62–66, https://doi.org/10.1016/j.mimet.2009.07.022.

    Article  Google Scholar 

  • Cardoso P H M, de Carvalho Balian S, Matushima E R, De Padua S B, Martins M L. 2017. First report of scuticociliatosis caused by Uronema sp. in ornamental reef fish imported into Brazil. Revista Brasileira de Parasitologia Veterinaria, 26(4): 491–495, https://doi.org/10.1590/s1984-29612017031.

    Article  Google Scholar 

  • Cawthorn R J, Lynn D H, Despres B, MacMillan R, Maloney R, Loughlin M, Bayer R. 1996. Description of Anophryoides haemophila n. sp. (Scuticociliatida: Orchitophryidae), a pathogen of American lobsters Homarus americanus. Diseases of Aquatic Organisms, 24(2): 143–148, https://doi.org/10.3354/dao024143.

    Article  Google Scholar 

  • Cheung P J, Nigrelli R F, Ruggieri G D. 1980. Studies on the morphology of Uronema marinum Dujardin (Ciliatea: Uronematidae) with a description of the histopathology of the infection in marine fishes. Journal of Fish Diseases, 3(4): 295–303, https://doi.org/10.1111/j.1365-2761.1980.tb00400.x.

    Article  Google Scholar 

  • Corliss J O. 1979. The Ciliated Protozoa. Characterization, Classification and Guide to the Literature. 2nd edn. Pergamon Press, Oxford, UK.

    Google Scholar 

  • Dyková I, Tyml T, Kostka M, Pecková H. 2010. Strains of Uronema marinum (Scuticociliatia) co-isolated with amoebae of the genus Neoparamoeba. Diseases of Aquatic Organisms, 89(1): 71–77, https://doi.org/10.3354/dao02168.

    Article  Google Scholar 

  • Edgar R C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5): 1 792–1 797, https://doi.org/10.1093/nar/gkh340.

    Article  Google Scholar 

  • Figueras A, Robledo D, Corvelo A, Hermida M, Pereiro P, Rubiolo J A, Gómez-Garrido J, Carreté L, Bello X, Gut M, Gut I G, Marcet-Houben M, Forn-Cuní G, Galán B, García J L, Abal-Fabeiro J L, Pardo B G, Taboada X, Fernández C, Vlasova A, Hermoso-Pulido A, Guigó R, Álvarez-Dios J A, Gómez-Tato A, Viñas A, Maside X, Gabaldón T, Novoa B, Bouza C, Alioto T, Martínez P. 2016. Whole genome sequencing of turbot (Scophthalmus maximus; Pleuronectiformes): a fish adapted to demersal life. DNA Research, 23(3): 181–192, https://doi.org/10.1093/dnares/dsw007.

    Article  Google Scholar 

  • Harikrishnan R, Balasundaram C, Heo M S. 2010. Scuticociliatosis and its recent prophylactic measures in aquaculture with special reference to South Korea: taxonomy, diversity and diagnosis of scuticociliatosis: part I Control strategies of scuticociliatosis: part II. Fish & Shellfish Immunology, 29(1): 15–31, https://doi.org/10.1016/j.fsi.2010.02.026.

    Article  Google Scholar 

  • Iglesias R, Paramá A, Alvarez M F, Leiro J, Fernández J, Sanmartín M L. 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, https://doi.org/10.3354/dao046047.

    Article  Google Scholar 

  • Jee B Y, Kim Y C, Park M S. 2001. Morphology and biology of parasite responsible for scuticociliatosis of cultured olive flounder Paralichthys olivaceus. Diseases of Aquatic Organisms, 47(1): 49–55, https://doi.org/10.3354/dao047049.

    Article  Google Scholar 

  • Kim S M, Cho J B, Kim S K, Nam Y K, Kim K H. 2004. Occurrence of scuticociliatosis in olive flounder Paralichthys olivaceus by Phiasterides dicentrarchi (Ciliophora: Scuticociliatida). Diseases of Aquatic Organisms, 62(3): 233–238, https://doi.org/10.3354/dao062233.

    Article  Google Scholar 

  • Medlin L, Elwood H J, Stickel S, Sogin M L. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71(2): 491–499, https://doi.org/10.1016/0378-1119(88)90066-2.

    Article  Google Scholar 

  • Ofelio C, Blanco A, Roura Á, Pintado J, Pascual S, Planas M. 2013. Isolation and molecular identification of the scuticociliate Porpostoma notata Moebius, 1888 from moribund reared Hippocampus hippocampus (L.) seahorses, by amplification of the SSU rRNA gene sequences. Journal of Fish Diseases, 37(12): 1 061–1 065, https://doi.org/10.1111/jfd.12207.

    Article  Google Scholar 

  • Piazzon M C, Leiro J, Lamas J. 2013. Fish immunity to scuticociliate parasites. Developmental & Comparative Immunology, 41(2): 248–256, https://doi.org/10.1016/j.dci.2013.05.022.

    Article  Google Scholar 

  • Qin L, Wang Y G, Zhang L J, Dai J X. 2007. Histopathology of turbot associated with Mesanophrys carcini parasite. Acta Hydrobiologica Sinica, 31(5): 618–628. (in Chinese with English abstract)

    Google Scholar 

  • Ramos M F, Costa A R, Barandela T, Saraiva A, Rodrigues P N. 2007. Scuticociliate infection and pathology in cultured turbot Scophthalmus maximus from the north of Portugal. Diseases of Aquatic Organisms, 74(3): 249–253, https://doi.org/10.3354/dao074249.

    Article  Google Scholar 

  • Song W B, Warren A, Hu X Z. 2009. Free-living Ciliates in the Bohai and Yellow Seas, China. Science Press, Beijing, China. p. 171–175. (in Chinese)

    Google Scholar 

  • 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, https://doi.org/10.1177/0300985813492800.

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis Version 6.0. Molecular Biology and Evolution, 30(12): 2 725–2 729, https://doi.org/10.1093/molbev/mst197.

    Article  Google Scholar 

  • Thompson Jr. J C, Moewus L. 1964. Miamiensis avidus n. g., n. sp., a marine facultative parasite in the ciliate order Hymenostomatida. Journal ofEukaryotic Microbiology, 11(3): 378–381, https://doi.org/10.1111/j.1550-7408.1964.tb01766.x.

    Google Scholar 

  • Turgay E, Steinum T M, Gül A E, Karataş S. 2015. An outbreak of scuticociliatosis in cultured common dentex (Dentex dentex) in turkey. Bulletin—European Association of Fish Pathologists, 35(3): 104–111.

    Google Scholar 

  • Wang Y G, Chen J J, Qin L. 2005. Mesanphrys carcini causing severe scuticociliatosis in farmed turbot Scophthalmus maximus in China. Journal of Fishery Sciences of China, 12(5): 594–601. (in Chinese with English abstract)

    Google Scholar 

  • Whang I, Kang H S, Lee J. 2013. Identification of scuticociliates (Pseudocohnilembus persalinus, P. longisetus, Uronema marinum and Miamiensis avidus) based on the cox1 sequence. Parasitology International, 62(1): 7–13, https://doi.org/10.1016/j.parint.2012.08.002.

    Article  Google Scholar 

  • Wilbert N. 1975. Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos, 64: 171–179.

    Google Scholar 

  • Zhang Z, Wang Y G, Qin L, Li Q F. 2006. Epizootic investigation and study on challenge experiment of fin rot disease in cultured turbot (Scophthalmus maximus). Fisheries Science, 25(6): 271–274. (in Chinese with English abstract)

    Google Scholar 

  • Zhou L, Zhan W B, Song W B, Song C H. 2000. Observations on the histopathology of the external ulcerative disease of Japanese flounder, Paralichthys olivaceus. Journal of Ocean University of Qingdao, 30(4): 593–597. (in Chinese with English abstract)

    Google Scholar 

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Acknowledgment

The LZLP2013 is morphologically identified by Prof. HU Xiaozhong and Dr. LIU Mingjian from the Laboratory of Protozoa, Ocean University of China.

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Author notes

  1. DU Guangxun and QU Lingyun contributed equally to this work.

Authors and Affiliations

  1. First Institute of Oceanography, Ministry of Natural Resources (MNR), Qingdao, 266061, China

    Guangxun Du, Lingyun Qu, Kun Shang, Chengjun Sun, Chen Wang & Ping Gao

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Lingyun Qu

  3. College of Fisheries and Life Science, Dalian Ocean University, Dalian, 116023, China

    Kun Shang

Authors
  1. Guangxun Du
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  2. Lingyun Qu
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  3. Kun Shang
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  4. Chengjun Sun
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  5. Chen Wang
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  6. Ping Gao
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Corresponding author

Correspondence to Lingyun Qu.

Additional information

6 Data Availability Statement

The 18S rRNA gene sequence of ciliate LZLP2013 is available from the National Center for Biotechnology Information under the accession number MF418591. The COX I gene sequence of ciliate LZLP2013 is available from the National Center for Biotechnology Information under the accession number MG372368.

Supported by the National Key R&D Program of China (No. 2017YFC1404504), the National Basic Research Program of China (973 Program) (No. 2015CB755904), the Scientific and Technological Innovation Project financially supported by Qingdao National Laboratory for Marine Science and Technology (Nos. 2015ASKJ02, 2016ASKJ14), and the Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology (No. 2016LMFS-B08)

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Du, G., Qu, L., Shang, K. et al. Ciliate Uronema marinum is the causative agent of scuticociliatosis in farm raised turbot Scophthalmus maximus. J. Ocean. Limnol. 37, 1726–1735 (2019). https://doi.org/10.1007/s00343-020-8305-8

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