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Morphological and Molecular Characterization of Ceratomyxa Batam N. Sp. (Myxozoa: Ceratomyxidae) Infecting the Gallbladder of Th

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Morphological and Molecular Characterization of Ceratomyxa Batam N. Sp. (Myxozoa: Ceratomyxidae) Infecting the Gallbladder of Th Parasitology Research (2019) 118:1647–1651 https://doi.org/10.1007/s00436-019-06217-w FISH PARASITOLOGY - SHORT COMMUNICATION Morphological and molecular characterization of Ceratomyxa batam n. sp. (Myxozoa: Ceratomyxidae) infecting the gallbladder of the cultured Trachinotus ovatus (Perciformes: Carangidae) in Batam Island, Indonesia Ying Qiao1 & Yanxiang Shao1 & Theerakamol Pengsakul 2 & Chao Chen1 & Shuli Zheng3 & Weijian Wu3 & Tonny Budhi Hardjo3 Received: 5 September 2017 /Accepted: 17 January 2019 /Published online: 23 March 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract A new coelozoic myxozoan species, Ceratomyxa batam n. sp., was identified in cultured carangid fish, Trachinotus ovatus (Perciformes: Carangidae), in waters off Batam Island of Indonesia. The bi- and trivalved spores were observed in the gallbladder of T. ovatus. Mature bivalved spores of C. batam n. sp. were transversely elongated and narrowly crescent in shape, 3.8 ± 0.36 (2.7–4.6) μm long and 19.2 ± 1.75 (16.2–22.0) μm thick. Two sub-spherical polar capsules were 2.3 ± 0.18 (2.0–2.8) μmlong and 2.6 ± 0.16 (2.3–2.9) μm wide. Prevalence was 72.2% in 72 examined T. ovatus according to evaluations dating from November 2016. The maximum likelihood phylogenetic tree based on small subunit rDNA sequence showed similarity with Ceratomyxa robertsthomsoni and Ceratomyxa thalassomae found in Australia. This is the first report of Ceratomyxa species identified in a seawater fish at Batam Island, Indonesia. Keywords Ceratomyxa Batam n. sp. Characterization . Parasite . Gallbladder . Trachinotus ovatus Introduction Cryptocaryonidae) (Dan et al. 2006), Paradeontacylix mcintosh (Trematoda: Sanguinicolidae), Benedenia diesing The Carangid fish ovate pompano (Trachinotus ovatus)isthe (Monogenea: Capsalidae), and Trichodibna ehrenberg most successfully cultured marine fish in the world. (Ciliophora: Peritrichida) (Xiong et al. 2015). Myxosporeans Nevertheless, in recent years, a range of fish-associated out- (Cnidaria: Myxozoa) are entozoic parasites that infect verte- breaks was caused by bacteria, virus or parasites (Dan et al. brates (fish, amphibians, rarely reptiles, birds, and mammals) 2006;Suetal.2015;Wangetal.2010). Trachinotus ovatus is and invertebrates (polychaete and oligochaete worms) world- considered as a susceptible host for many marine parasites wide. The genus Ceratomyxa Thelohan, 1892 is among the such as Cryptocaryon irritans (Prorodontida: more diverse myxosporean genera and includes more than 300 reported species (Lom and Dyková 2006). Species be- longing to the genus Ceratomyxa are characterized by mature Section Editor: Christopher Whipps spores with the following morphological structures: crescent or arcuate shaped and with elongate shell valves that are gen- * Chao Chen erally thicker than the length (Lom and Dyková 2006). [email protected] Members of the Ceratomyxidae Doflein, 1899 within the or- der Myxosporea are mainly considered parasites of marine 1 Yellow Sea Fisheries Research Institute, Chinese Academy of teleosts and are rarely reported in freshwater fish (Lom and Fishery Sciences, Nanjing road, Qingdao 266071, Shandong Province, People’s Republic of China Dyková 2006). Pathogenic potentials of Ceratomyxa species are very rarely documented (Feist and Longshaw 2005). Prior 2 Faculty of Medical Technology, Prince of Songkla University, Hat Yai, Songkhla 90110, Thailand to being reassigned as Ceratonova shasta, Ceratomyxa shasta was one of the best known pathogenic Ceratomyxa species 3 PT. CAHAYATERANG SEJATI, Batam Island, Riau Province, Indonesia which caused significant losses to salmonid aquaculture in 1648 Parasitol Res (2019) 118:1647–1651 North America (Bartholomew et al. 1989;Bowerand The small subunit (SSU) rDNA was amplified via PCR Margolis 2002). In addition, Maita et al. (1997) suspected a using forward primer MyxospecF (5′-TTC TGC CGT ATC myxosporean may have been associated with the green liver AAC TWG TTG-3′)(Fiala2006) and reverse primer18R symptom in Seriola quinqueradiata. A subsequent survey by (5′-CTA CGG AAA CCT TGT TAC G-3′) (Whipps et al. Yokoyama and Fukuda (2001) identified two Ceratomyxa 2003). PCR reactions were performed in a total reaction species, but pathological changes were not apparent (Maita volume of 25 μl, containing 15 μl of PCR-grade ddH2O, et al. 1997; Yokoyama and Fukuda 2001). During the process- 2.5 μl of 10× PCR buffer, 0.1 mM dNTP mix (2.5 mM), ing stage of cultured T. ovatus in Batam Island, Indonesia, we 0.4 μM each primer (10 mM), 1.5 U Taq polymerase identified a new myxosporean in the gallbladder of T. ovatus, (Takara), and 0.5 μg of DNA. PCR amplification parame- and we described in detail its morphology and phylogenetic ters were as follows: 1 cycle of 95 °C for 5 min, 30 cycles relationships. of 95 °C for 30 s, 50 °C for 30 s, and 72 °C for 60 s, followed by the final extension at 72 °C for 7 min. The PCR products were separated by electrophoresis on a 1% Materials and methods agarose gel, visualized on a UV transillumination system (Tanon-3500R), and fragments excised and purified using Host fish and parasite sampling EasyPure Quick Gel Extraction Kit (TRANSGEN BIOTECH). PCR products were sequenced at Shanghai In November 2016, 72 cultured T. ovatus were collected from Sangon Company (Shanghai, China) using a pair of inter- the aquaculture area off Batam Island, Indonesia (0° 38’ 19’’ nal primers, MyxF (5′-GAC TCA ACA CGG GAA AAC N104°15’ 23’’ E). The gallbladders of T. ovatus were re- TTA-3′) and MyxR (5′-TGG CCG TTC TTA GTT CGT moved, and the bile was examined for myxosporean infec- GGA GTG AT-3′)(Mansouretal.2013). tions using light microscopy. Fresh spores were photographed and measured using a Nikon Eclipse Ci microscope. The de- scription and measurements of spores (n = 30) were made fol- Phylogenetic analysis lowing the guidelines of Lom and Arthur (1989) and Heiniger et al. (2008)(Fig.1). For Giemsa stain preparation, the spores For phylogenetic analysis, the obtained SSU rDNA se- were fixed in absolute methanol for 10 min, air dried, and then quence was queried at National Center for Biotechnology stained using Giemsa stain solution (Solarbio, G4640), fol- Information (NCBI) (http://www.ncbi.nlm.nih.gov/) using lowing the manufacturer’s instruction. For DNA extraction, the Basic Local Alignment Search Tool. Taxa with similar positive gallbladders (n = 5) were preserved in absolute etha- DNA sequence and similar morphology were selected for nol and were then stored in − 20 °C. phylogenetic analysis. The multiple sequence alignment was performed using ClustalX2 with other homologous Small subunit ribosomal DNA amplification sequences. The maximum likelihood (ML) phylogenetic tree was generated using online PhyML 3.0 (http://www. When myxosporea species were detected, 100 μlofethanol- atgc-montpellier.fr/phyml/) with Smart Model Selection preserved bile was pelleted and washed three times in ddH2O. (Guindon et al. 2010). An Akaike Information Criterion DNA was extracted using the DNeasy Blood & Tissue Kit (AIC) model was selected, and subtree pruning and (Qiagen Inc., Valencia, CA) following the manufacturer’sin- regrafting (SPR) was selected as the type of tree improve- structions. The extracted DNA was then stored at − 20 °C. ment. The number of bootstrap replicates was 100. Fig. 1 Schematic diagram of spore measurements (Heiniger et al. 2008). L, length; PA, posterior angle, PCL, polar capsule length; PCW, polar capsule width; S, sutural position; T, thickness of cultured Fig. 2 Indonesia. Mature spores of T. ovatus Bi- and trivalved spores were observed in the bile of cultured Morphological description of spores Ceratomyxa batam Results Parasitol Res (2019) 118:1647 the genus line (Fig. valves had one polar capsuleconvex with anterior equal end size and near a the concaveunequal sutural posterior valves end. by Both the spore straight suturalrowly line, crescent forming shape. a Mature slightly spores were separated into two long and 19.2 ± 1.75 (16.2 2.8) spherical polar capsules were equal in size (2.3 ± 0.18 (2.0 trivalved spore of angle was 162.3° ± 5.39° (155.4 Giemsa-stained trivalved spore of shaped trivalved spores (Fig. amounts in the bile of the cultured ovatus Taxonomic summary examined of 104° 15 Type host-locality: Batam Island, Indonesia (0° 38 Site of infection: Within gallbladder. C. batam μ The fresh spores of m long and 2.6 ± 0.16 (2.3 (Perciformes: Carangidae) (Linnaeus, 1758). ’ T. ovatus 23 Ceratomyxa T. ovatus. 2 (Perciformes: Carangidae) from Batam Island, a). Mature spores were 3.8 ± 0.36 (2.7 ’’ n. sp. in November 2016 was 72.2% in the 72 E). C. batam a Fresh spore of Type host: Ovate pompano, Ceratomyxa batam n. sp. with a transversely elongated and nar- – 1651 n. sp. – C. batam C. batam 22.0) 2 b) were also observed in small C. batam c Giemsa-stained free spores. – – T. ovatus 2.9) μ 175.2°) (Table m thick. The two sub- n. sp. Scale bar = 10 n. sp. from the gallbladder n. sp. were typical of n. sp. μ m wide). Posterior . The prevalence b Fresh Trachinotus B – Y 4.6) 1 ^ ’ ). -shaped μ 1 m B ’’ μ Y m N – ^ d Table 1 Comparative morphological description of Ceratomyxa batam n. sp. with similar species (measurements in μm) Name Hosts Locality L T PCL PCW PA References (Ceratomyxa spp.) C. batam n. sp. Trachinotus ovatus Indonesia 3.8 ± 0.36 (2.7–4.6) 19.2 ± 1.75 (16.2–22.0) 2.3 ± 0.18 (2.0–2.8) 2.6 ± 0.16 (2.3–2.9) 162.3 ± 5.39 (155.4–175.2) Present research C. tunisiensis Caranx rhonchus, Gulf of Gabes, 6 ± 0.26 (5–8) 23 ± 0.27 (20–25) N N N Thabet et al. (2016) Trachurus trachurus Tunisia C. seriolae Seriola quinqueradiata Japan 6.5 (6.0–7.5) 33.7 (28.0–41.5) 1.9 (1.5–2.0) N N Yokoyama and C.
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