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Phylogeny of Myxobolidae (Myxozoa) and the Evolution of Myxospore

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Phylogeny of Myxobolidae (Myxozoa) and the Evolution of Myxospore International Journal for Parasitology 49 (2019) 523–530 Contents lists available at ScienceDirect International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara Phylogeny of Myxobolidae (Myxozoa) and the evolution of myxospore appendages in the Myxobolus clade ⇑ ⇑ Yang Liu a,b, Alena Lövy c, Zemao Gu a,b, , Ivan Fiala c,d, a Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China b Hubei Engineering Technology Research Center for Aquatic Animal Diseases Control and Prevention, Wuhan 430070, China c Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 Cˇeské Budĕjovice, Czech Republic d Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 Cˇeské Budĕjovice, Czech Republic article info abstract Article history: Genera Myxobolus Bütschli, 1882 and Henneguya Thélohan, 1892 (Myxobolidae) are specious myxozoan Received 15 November 2018 genera. They comprise nearly half of overall known myxozoan species diversity. A typical spore feature of Received in revised form 28 January 2019 Henneguya is the presence of two caudal appendages of the spore valves, which distinguishes them from Accepted 3 February 2019 species of the genus Myxobolus. Several Myxobolus spp., however, were reported to show aberrant spores Available online 9 May 2019 with Henneguya-like caudal appendages. We found such aberrant spores in Myxobolus tsangwuensis and Myxobolus wulii. We studied the ultrastructure of M. wulii and Myxobolus oralis spores with caudal appen- Keywords: dages by transmission electron microscopy (TEM). TEM of these aberrant spores revealed that their cau- Myxobolus dal appendages have the same ultrastructure as the appendages of Henneguya spp. Small caudal Henneguya Character evolution appendages of M. wulii spores observed only on TEM suggested that this character may be often over- Ultrastructure looked and more Myxobolus species potentially have the ability to express the caudal appendages on Phylogenetic analysis the myxospore. In order to trace the evolution of this character, we performed broad phylogenetic anal- ysis of all species of the family Myxobolidae which are available in GenBank including nearly 300 taxa. We found at least eight independent evolutionary origins of spores with two appendages, three origins of a single appendage and 12 apparent secondary losses of the spore projections. Therefore, genus Henneguya with typical two-tailed myxospores is polyphyletic, however a majority of its species has a common ancestor and groups in the second largest subclade of the Myxobolus clade. We also mapped the biological characteristics (host, site of infection and environment) of Myxobolidae species on the phy- logenetic tree. We revealed an evident host-associated evolutionary pattern in all parts of the Myxobolus clade with a distinct and species-rich subclade containing almost exclusively species infecting species of the Order Cypriniformes. Ó 2019 Australian Society for Parasitology. Published by Elsevier Ltd. All rights reserved. 1. Introduction an invertebrate definitive host (typically oligochaete or poly- chaete) that releases actinospore stages, which are infective to Myxosporeans are a morphologically and biologically diverse the vertebrate intermediate host, to complete the life cycle (Wolf group of cnidarian endoparasites with approximately 2600 species and Markiw, 1984). described (Okamura et al., 2018). Most of them infect aquatic ani- Myxosporean taxonomy is mostly based on myxospore mor- mals, especially fish, and less frequently other poikilothermic and phology, mainly the number and configuration of shell valves homoeothermic vertebrates such as amphibians, reptiles, birds and polar capsules (Shulman, 1966; Lom and Noble, 1984). Classi- and mammals (Friedrich et al., 2000; Eiras, 2005; Prunescu et al., fication also takes into account many additional details of the myx- 2007; Bartholomew et al., 2008). Myxosporean life cycles require ospore structure as described by Lom and Arthur (1989), such as the presence of caudal projections, the presence of ribs, ridges and striations on the spore valves, the number of turns of polar fil- ⇑ Corresponding authors at: Department of Aquatic Animal Medicine, College of ament, the mutual size relation of polar capsules or the presence of Fisheries, Huazhong Agricultural University, Wuhan 430070, China. Fax: +86 27 a mucous envelope, the number of sporoplasms etc. Most of these 87282114 (Zemao Gu). Institute of Parasitology, Biology Centre, Academy of morphological details are important for differentiation of myx- Sciences of the Czech Republic, Branišovská 31, 370 05 Cˇeské Budĕjovice, Czech Republic. Fax: +420 385310388 (I. Fiala). osporeans at the species level. One of the exceptions is the pres- E-mail addresses: [email protected] (Z. Gu), fi[email protected] (I. Fiala). ence/absence and the nature of myxospore caudal projections https://doi.org/10.1016/j.ijpara.2019.02.009 0020-7519/Ó 2019 Australian Society for Parasitology. Published by Elsevier Ltd. All rights reserved. 524 Y. Liu et al. / International Journal for Parasitology 49 (2019) 523–530 which are the main distinguishing character of the genus Myxobo- 2009–2013 (Table 1). Samples were checked carefully by micro- lus, Henneguya, Hennegoides and Unicauda (Lom and Dyková, 2006). scopic observation to ensure that they contained spores of only Myxobolus Bütschli, 1882 and Henneguya Thélohan, 1892 are one species. Light microscopy was performed on an Olympus the most species rich genera within the Myxozoa. Almost half of BX53 microscope (Olympus optical Co. Ltd., Japan) equipped with the myxozoan diversity is concentrated into these two genera with an Olympus DP73 camera (Olympus optical Co. Ltd., Japan). more than 850 Myxobolus spp. (Eiras et al., 2014) and 200 species of the genus Henneguya (Eiras and Adriano, 2012) described. Taxo- 2.2. Ultrastructural examination nomically, they are classified to the family Myxobolidae including another 12 genera with similar spore morphology and the prefer- Isolated spores of M. oralis, Myxobolus wulii and Henneguya ence of infecting tissues rather than body cavities of freshwater doneci were fixed in 3% glutaraldehyde (Sigma-Aldrich, St. Louis, fishes. They can produce large polysporic plasmodia in the tissues USA) in 0.2 M sodium cacodylate (SINOPHARM, Shanghai, China) and may cause severe diseases (Lom and Dyková, 2006). Fourteen buffer (pH 7.2) at 4 °C overnight and post-fixed in 2% OsO4 (Green- genera of Myxobolidae differ by the number of polar capsule(s) and light, Beijing, China) buffered with the same solution for 4 h at the the presence and number of spore projection(s) (Lom and Dyková, same temperature. Following an ethanol series and propylene 2006; Sarkar, 2009). Myxobolus spp. are characterized by the ellip- oxide dehydration, samples were embedded in Epon812 (Emicron, soidal or rounded spores with two polar capsules lying in the sutu- Shanghai, China). Semithin sections were stained with Toluidine ral plane. Spores of Henneguya spp. are similar to those of blue (Sigma-Aldrich, St. Louis, USA). Ultrathin sections, double con- Myxobolus, differing only in the presence of two caudal appen- trasted with uranyl acetate and lead citrate, were observed using a dages. These structures represent valve extensions at the posterior HITACHI H-7650 transmission electron microscope (Hitachi, part of the spore. The Myxobolus spore morphotype is simple and Tokyo, Japan) at 75 kV. can be considered a primary morphotype within Myxobolidae from which other spore morphotypes such as Henneguya (two cau- 2.3. DNA isolation, PCR and sequencing dal appendages), Unicauda (one caudal appendage) or Thelohanellus (reduced polar capsule) evolved (Fiala and Bartošová, 2010). Genomic DNA was extracted from fresh spores or the samples Molecular taxonomy based on the ssrRNA gene does not sup- fixed in 100% ethanol using a BioTekeTM Genomic DNA extraction port the classical spore-based taxonomic classification of Myxobol- kit (BioTeke Co., Ltd, Beijing) according to the manufacturer’s pro- idae (e.g. Kent et al., 2001; Fiala, 2006; Fiala and Bartošová, 2010). tocol. The ssrRNA gene was PCR amplified with a set of universal In phylogenetic trees, the positions of many species often disagree eukaryotic primers (18e, 5-CTGGTTGATTCTGCCAGT-3 (Hillis and with the expected relationships deduced from the taxonomy based Dixon, 1991) and 18R, 5-CTACGGAAACCTTGTTACG-3 (Whipps on the spore morphology. Kent et al. (2001) already speculated, in et al., 2003)) to obtain an almost complete sequence. PCR was car- their first broad phylogenetic analysis of the Myxosporea, that the ried out in a 50 ll reaction volume containing approximate 200 ng caudal appendages of Henneguya spp. were not a valid feature for a of extracted genomic DNA, 1ÂTaq Buffer (MBI Fermentas, Vilnius, characterization of the genus. Increasing numbers of available Lithuania), 2.5 mM MgCl2, 0.2 mM dNTPs (MBI Fermentas), 2 lM sequence data supported the paraphyletic character of the genus each primer, and 2.5 U of Taq DNA polymerase (MBI Fermentas) Myxobolus with a number of Henneguya spp. clustering within in MilliQ purified water. An EDC-810 DNA Engine (EastWin Bio., the Myxobolus clade (e.g. Fiala, 2006; Liu et al., 2010). Co., Ltd, Beijing) was used to control the cycling conditions: 95 °C Eszterbauer (2004) found that the preference for a particular site for 50 s, 48 °C for 50 s, and 72 °C for
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