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Full Text in Pdf Format Vol. 141: 39–46, 2020 DISEASES OF AQUATIC ORGANISMS Published online September 17 https://doi.org/10.3354/dao03514 Dis Aquat Org Morphological, histological and molecular characterization of Myxidium cf. rhodei infecting the kidney of Rutilus rutilus Marina Dashi-Dorjievna Batueva1,#, Xiaoyi Pan2,#, Jinyong Zhang3,4, Xinhua Liu3, Wu Wei3, Yang Liu3,4,* 1Institute of General and Experimental Biology of the Siberian Branch of the Russian Academy of Sciences, 670047 Ulan-Ude, Russia 2Key Laboratory of Healthy Freshwater Aquaculture, Ministry of Agriculture and Rural Affairs; Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, 313001 Huzhou, PR China 3Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture and Rural Affairs; State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, 430072 Wuhan, PR China 4School of Marine Science and Engineering, Qingdao Agricultural University, 266109 Qingdao, PR China ABSTRACT: In the present study, we provide supplementary data for Myxidium cf. rhodei Léger, 1905 based on morphological, histological and molecular characterization. M. cf. rhodei was ob - served in the kidneys of 918 out of 942 (97%) roach Rutilus rutilus (Linnaeus, 1758). Myxospores of M. cf. rhodei were fusiform with pointed ends, measuring 12.7 ± 0.1 SD (11.8−13.4) μm in length and 4.6 ± 0.1 (3.8−5.4) μm in width. Two similar pear-shaped polar capsules were positioned at either ends of the longitudinal axis of the myxospore: each of these capsules measured 4.0 ± 0.1 (3.1−4.7) μm in length and 2.8 ± 0.1 (2.0−4.0) μm in width. Polar filaments were coiled into 4 to 5 turns. Approximately 18−20 longitudinal straight ridges were observed on the myxospore surface. The suture line was straight and distinctive, running near the middle of the valves. Histologically, the plasmodia of the present species were found in the Bowman’s capsules, and rarely in the inter- stitium of the host. Phylogenetic analysis revealed that M. cf. rhodei was sister to M. anatidum in the Myxidium clade including most Myxidium species from freshwater hosts. KEY WORDS: Myxidium cf. rhodei · Rutilus rutilus · Myxosporea · Kidney · SSU rDNA Resale or republication not permitted without written consent of the publisher 1. INTRODUCTION torical and technical reasons, most of the reported myxosporean species have been described solely Myxosporeans are a group of morphologically and by myxospore morphology (Eiras et al. 2011), which biologically diverse cnidarian endoparasites that pri- makes accurate identification and discrimination of marily infect both freshwater and marine fishes, with species challenging. Recently, biological traits (host over 2600 species described throughout the world specificity, organ specificity, and tissue tropism) and (Okamura et al. 2018). Of these, Myxidium Bütschli, molecular characterization have been suggested to 1882 represents a species-rich genus including over provide more accurate myxosporean species discrim- 230 nominal species recorded (Eiras et al. 2011, ination and identification (Atkinson et al. 2015). Un - Espinoza et al. 2017, Fariya et al. 2020). Most Myxid- fortunately, molecular data for most myxosporean ium species are typically coelozoic and generally species are lacking. Small subunit ribosomal DNA develop in the gallbladder, urinary bladder, or uri- (SSU rDNA) sequences are available for only ~30 of nary tubules of fish hosts (Eiras et al. 2011). For his- the Myxidium spp. reported to date. *Corresponding author: [email protected] © Inter-Research 2020 · www.int-res.com # These authors contributed equally to this work 40 Dis Aquat Org 141: 39–46, 2020 Myxidium rhodei Léger, 1905 is an economically Donets & Shul’man (1973). Morphological and mor- important myxosporean parasite primarily infecting phometric analyses of myxospores were carried out the kidney of fish hosts. It was described for the first using Carl Zeiss Axio Lab.A1 (Carl Zeiss Microscopy) time from the kidney and ureter of Rhodeus amarus with Nikon-Elements BR software according to Lom (Bloch, 1782) in France (Léger 1930). Subsequently, & Arthur (1989). All measurements are given in micro - infections of M. rhodei were reported from more than meters (μm) as mean ± SD, followed by range in 40 freshwater fish species with a wide geographical parentheses. distribution (Jaysari & Hoffman 1982, Shul’man 1984, For scanning electron microscopy, myxospores Dyková et al. 1987, Alvarez-Pellitero 1989, Kepr 1991, were transferred to a poly-L-lysine-coated coverslip Athanassopoulou & Sommerville 1993a,b, Chen & Ma and allowed to stand for 15 min, then fixed in 2.5% 1998, Longshaw et al. 2005, Pazooki & Masoumian glutaraldehyde buffered in 0.1 M sodium cacodylate 2012). Although most of these infections were reported buffer (pH 7.4) at 4°C for 24 h, and then dehydrated from the kidneys of hosts, other organs including gills, in a series of increasing concentrations of ethyl al- muscle, liver, spleen, heart, gallbladder, intestine, cohol. Finally, coverslips were critical point dried swim bladder, gonads, urinary bladder, and ureter and broken on a stub before coating with gold. The have also been recorded as infection sites of M. rhodei fixed myxospores were observed and photographed (Kepr 1991, Athanassopoulou & Sommerville 1993b, using a Hitachi S-800 SEM with TM-1000 Ver.02-01 Chen & Ma 1998). Given the many detections of M. software. rhodei from various organs of more than 40 fish species that were identified by myxospore morphology alone, the reliability of M. rhodei species identification is 2.3. Histopathology questionable (Longshaw et al. 2005). Therefore, it is not clear whether M. rhodei is a widely distributed Infected kidney tissue of 50 fish collected during parasite infecting various organs of diverse fishes or 2016− 2018 was fixed in 4% formalin over 24 h, whether some infections represent other morphologi- gradient- dehydrated, embedded in paraffin, sec- cally similar but different myxosporean species. tioned at 5−6 μm, stained with hematoxylin and To facilitate the accurate species identification of eosin, and then examined and photographed with M. rhodei, here we provide supplementary morpho- a Carl Zeiss Axio Lab.A1 with Nikon-Elements BR logical, histological, and molecular characterization software. All measurements are given in μm. of M. cf. rhodei. 2.4. DNA extraction, amplification, and sequencing 2. MATERIALS AND METHODS Genomic DNA was extracted using the DNeasy 2.1. Fish collection Blood & Tissue Kit (Qiagen), following the manu- facturer’s recommended protocol for animal tissue. A total of 942 roach Rutilus rutilus individuals were PCR amplification of SSU rDNA sequence was per- caught by gill nets from Chivyrkui Bay (53° 46’ N, formed using the primer pair MyxospecF (Fiala 2006) 109° 02’ E) in Lake Baikal, Russia, during all 4 seasons and 18R (Whipps et al. 2003). PCR was carried out in from 2008 to 2018. All specimens were transported a 25 μl reaction mixture, containing 30 ng of ex - alive to the laboratory and euthanized by an overdose tracted genomic DNA, 1× PCR mixture (CWBiotech), of tricaine methanesulfonate (MS222, Sigma) buffered and 10 pmol of each primer. The PCR reaction was with bicarbonate. Comprehensive examination of the performed with initial denaturation for 4 min at 95°C, skin, fins, gills, muscle, intestine, liver, spleen, swim followed by 35 cycles of denaturation at 95°C for bladder, gallbladder, kidney, heart, gonads, urinary 1 min, annealing at 48°C for 1 min, extension at 72°C bladder, and ureter for myxosporean infections were for 2 min, and a final elongation step at 72°C for performed by gross examination and light microscopy. 10 min. The amplified PCR products were excised from an agarose gel, purified using a PCR purifica- tion kit (CWBiotech), and cloned into the PMD18-T 2.2. Morphological examination vector system (Takara). Positive clones were then selected and sequenced in both directions using the Fresh myxospores of Myxidium cf. rhodei were fixed amplification primers from the ABI BigDye Termi - in glycerol-gelatin as a slide preparation according to nator v 3.1 Cycle Sequencing Kit with an ABI 3100 Batueva et al.: Supplementary data for Myxidium cf. rhodei 41 Genetic Analyzer. The contiguous sequences were with 6 rate categories. BI analysis was conducted in assembled according to the corresponding chroma - ‘MrBayes’ v.3.2.6 (Ronquist et al. 2012), with 106 gen- tograms with the SeqMan™ utility of the ‘Lasergene’ erations, tree sampling every 100 generations, with a software package (DNAStar) and submitted to the burn-in of 2500 trees. ML analysis was performed National Center for Biotechnology Information nucleo - using ‘PhyML’ 3.0 (Guindon et al. 2010). Bootstrap tide database. confidence values were calculated with 1000 repli- cates. Trees were initially examined in ‘FigTree’ v1.3.1 (http://tree.bio.ed.ac.uk/software/figtree/) and then 2.5. Phylogenetic analysis edited and annotated in Adobe Illustrator (Adobe Systems). To explore the phylogenetic relationship of the present species with the existing myxosporean spe- cies, 49 SSU rDNA sequences of myxosporeans were 3. RESULTS obtained from GenBank and aligned with ClustalX 1.8 (Thompson et al. 1997) using the default setting. 3.1. Morphological description Tetracapsuloides bryosalmonae (U70623) was chosen as the outgroup taxon. Phylogenetic trees were con- Plasmodia of Myxidium cf. rhodei were observed structed using maximum likelihood (ML) and Bayesian in the kidneys of 918 out of 942 (97%) Rutilus rutilus. (BI) analyses. The optimal evolutionary model for ML Myxospores of M. cf. rhodei were fusiform with and BI analyses was determined using ‘jModeltest’ pointed ends (Figs. 1 & 2), measuring 12.7 ± 0.1 3.7 (Posada 2008), which identified the optimal evo- (11.8−13.4) in length and 4.6 ± 0.1 (3.8−5.4) in width. lutionary model as the general time-reversible model Two equal pear-shaped polar capsules were posi- using Akaike’s information criterion.
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