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Kudoa Thyrsites from Japanese Flounder and Kudoa Lateolabracis N. Sp. from Chinese Sea Bass: Causative Myxozoans of Post-Mortem Myoliquefaction

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Kudoa Thyrsites from Japanese Flounder and Kudoa Lateolabracis N. Sp. from Chinese Sea Bass: Causative Myxozoans of Post-Mortem Myoliquefaction 魚 病 研 究Fish Pathology,39(2),79-85,2004.6 2004 The Japanese Society of Fish Pathology Kudoa thyrsites from Japanese Flounder and Kudoa lateolabracis n. sp. from Chinese Sea Bass: Causative Myxozoans of Post-Mortem Myoliquefaction Hiroshi Yokoyama1*, Christopher M. Whipps2, Michael L. Kent2, Kaori Mizuno3 and Hidemasa Kawakami3 1 Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo 113-8657, Japan 2Center for Fish Disease Research , Department of Microbiology, Oregon State University, Corvallis, Oregon 97331-3404, USA 3 Ehime Prefectural Fish Disease Control Center , Uwajima, Ehime 798-0087, Japan (Received November 17, 2003) ABSTRACT--Post-mortem myoliquefaction caused by myxozoans of the genus Kudoa was observed in Japanese flounder Paralichthys olivaceus and Chinese sea bass Lateolabrax sp. cultured in Japan. Morphological and molecular analyses of the myxozoan from Japanese floun der identified it as Kudoa thyrsites, which has been described from various marine fishes in different oceans. The parasite from Chinese sea bass was similar to K. thyrsites, having stellate spores with one polar capsule larger than the other three. However, the spore size was smaller than that of K. thyrsites. The small subunit rDNA sequence from the Kudoa sp. of Chinese sea bass was distinct from that of K. thyrsites and phylogenetic analysis placed it as an outlier to K. thyrsites. Therefore, we describe the myxozoan from Chinese sea bass as Kudoa lateolabracis n.sp. Key words: myxozoan, Kudoa thyrsites, Kudoa lateolabracis, Paralichthys olivaceus, Lateolabrax sp., Japanese flounder, Chinese sea bass, myoliquefaction Post-mortem myoliquefaction, commonly referred to Atlantic herring (Clupea harengus), K. cruciformum in as 'soft flesh','milky condition' or 'jellied meat' of wild Japanese sea bass (Lateolabrax japonicus), K. funduli in and cultured fishes is a well-known disease which is mummichog (Fundulus heteroclitus), K. histolytica in caused by myxozoan parasites, mostly belonging to the Atlantic mackerel (Scomber scombrus), K. mirabilis in genus Kudoa. Muscle degeneration is due to the pro ribbonfish (Trichiurus haumela), K. musculoliquefaciens teolytic enzymes possibly released from the pre in swordfish (Xiphias gladius), K. paniformis in Pacific sporogonic plasmodia of the parasite (Stehr and hake (Merluccius productus), K. peruvianus in Chilean Whitaker, 1986). Although there was no observable ef hake (Merluccius gayi), K. rosenbuschi in Argentine fect on physiology, behavior, or survival of the host fish, hake (Merluccius hubbsi) and K. thyrsites in farmed Kudoa infections have been of concern to aquaculture Atlantic salmon (Salmo salar) and various marine fishes. and commercial fisheries due to their negative impact on Since the late 1980's, aquaculture of Japanese product quality (Moran et al., 1999a). Kudoa is com flounder (Paralichthys olivaceus) has expanded rapidly, prised of more than 40 identified species (Moran et al., and its annual production has reached approximately a; Swearer and Robertson, 1999), and the following1999 7,000 metric tons in recent years. Japanese flounder is have been reported as causative agents of post-mortem usually raised in land-based tanks with running seawa myoliquefaction (Moran et al., 1999a): K. clupeidae in ter, and on occasion, several parasitic infections, e.g., ciliates and monogeneans, have become fatal problems * Corresponding author (Ogawa and Yokoyama, 1998). Accompanied by diver E-mail: [email protected] sification of cultured fish species, growing interest of 80 H. Yokoyama, C. M. Whipps, M. L. Kent, K. Mizuno and H. Kawakami Chinese sea bass (Lateolabrax sp.) culture has led to cession numbers. Briefly, polymerase chain reaction the increased importation of seedlings to Japan from (PCR) primers and procedures of Whipps et al. (2003) China. As opposed to the Japanese sea bass were used to amplify overlapping fragments of SSU (Lateolabrax japonicus), Chinese sea bass has a greater rDNA. Fragments were sequenced in both directions tolerance to brackish or fresh water and a faster growth using PCR primers with AP Biotech(r) DYEnamic ET rate, suggesting that it is a promising species for marine Terminator cycle sequencing chemistry with Thermo finfish aquaculture. Sequenase II (Amersham Biosciences, USA) on an ABI Recently, muscle liquefaction was observed in fillets PRISM(r) 377 DNA Sequencer (Applied Biosystems, of cultured Japanese flounder and Chinese sea bass, USA). and stellate Kudoa spores were detected in these in Myxozoan small subunit (SSU) sequences for avail fected tissues. In the present study, we conducted able for members of the order Multivalvulida of approxi morphological and molecular analyses of the parasites mately 1600 bp were aligned with ClustaIX (Thompson with the aim of identifying the causative organisms. et al., 1997) and examined by eye. A single variable sequence region of approximately 100 bp was realigned with Malign (Wheeler and Gladstein, 1994) with 10 Materials and Methods random sequence additions, an internal gap cost of 3, Fish sampling extra gaps cost 1, and tree bisection and reconnection Fillets of Japanese flounder (body weight, ca. 800 g) branch swapping. The following sequences (with showing the muscle degeneration were brought to our GenBank accession numbers) were used: Ceratomyxa laboratory from a processing company in Ehime Prefec shasta (AF001579), Kudoa amamiensis (AF034638), ture, western Japan, on January 10th and May 7th, Kudoa crumena (AF378347), Kudoa dianae 2003. The seedlings of Japanese flounder were im (AF414692), Kudoa lateolabracis n. sp. (AY382606), ported to Japan from Korea about one year before the Kudoa miniauriculata (AF034639), Kudoa minithyrsites harvest and then farmed in land-based tanks in Ehime (AY152749), Kudoa ovivora (AY152750), Kudoa Prefecture. Samples of liquefied Chinese sea bass paniformis (AF034640), Kudoa permulticapsula (body weight, ca. 2.3 kg) were transferred to our labora (AY078429), Kudoa quadricornis (AY078428), Kudoa tory on March 6th and June 30th, 2003. The seedlings shiomitsui (AY302724), Kudoa sp. from southern floun of Chinese sea bass were imported from China and der (Paralichthys lethostigma) (AY302723), K. thyrsites cultured in sea-cages in the Seto Inland Sea off Ehime from mahi mahi (Coryphaena hippurus) (AY152747), Prefecture. Incidence of •esoft flesh' (generalized K. thyrsites from Salmo salar (AF031412), K. thyrsites muscle liquefaction or even several pale foci) was exam from Thyrsites atun (AY078430), K. thyrsites from ined by visual observation and defined as the number of Japanese flounder (AY382607), Pentacapsula fish with liquefied area per the number of fish neurophila (AY172511), Hexacapsula sp. ex Gram examined. Prevalence of infection, the number of fish matorcynus bicarinatus (AY302723), Hexacapsula infected per number of fish examined, was determined sp. ex Scomberomorus commerson (AY302739), by microscopic observation for the presence of spores. Hexacapsula sp. ex Thalassoma lunare (AY302738), Infected muscle tissues were preserved in frozen for Septemcapsula yasunagai (AY302741) . morphological examination, in 10% formalin for histol Phylogenetic analyses of aligned sequences was ogy, and in 95% ethanol for DNA analysis. conducted using PAUP*4.0b1 (Swofford, 1998). Parsi mony analysis used the heuristic search algorithm with Morphological examination 50 random additions of sequences and tree bisection Thawed muscle tissues were examined macro reconnection (TBR) branch swapping. Bootstrap val scopically and followed by wet-mount preparations of ues were calculated with 1000 replicates using the heu muscle lesions using agar-coated slides for light micro ristic search algorithm with simple sequence addition scopical observations. Descriptions and measure and TBR branch swapping. Distance and maximum ments were made according to Lom and Arthur (1989) likelihood analyses were also performed. Distances and Langdon (1991). Formalin-fixed tissues from Chi were calculated using the HKY85 evolutionary model nese sea bass were processed by routine histology, and and a tree was constructed with the neighbor-joining paraffin sections cut at 5 ƒÊm thick were stained with H & method. Maximum likelihood (ML) also employed the E or Diff-Quik and observed by light microscopy. HKY85 model and a heuristic search algorithm with 10 random sequence additions and TBR branch swapping. Molecular analysis Bootstrap values were calculated with 100 replicates for Small subunit rDNA sequence of approximately MI trees distance and 1680 bp was obtained for K. thyrsites from Japanese flounder and K. lateolabracis n. sp. from Chinese sea bass and deposited in GenBank with the following ac Kudoa causing myoliquefaction 81 able among the host species and the localities (Table Results 1) Spores from Chinese sea bass closely resemble to Diagnosis those of K thyrsites, having stellate spores with one po Based on visual observations of 'soft flesh' in har lar capsule larger than the other three (Figs 3 and vested fish, the incidence in Japanese flounder 4) However, they were clearly smaller than those of K appeared to be very low (less than 1%), whereas that in thyrsites and showed considerable differences in Chinese sea bass was 15% (3 out of 20) at one farm SSU rDNA sequence We, therefore, described the site No marked variation of disease incidence in differ myxozoan from Chinese sea bass as a new species ent localities was observed
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