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A Horsehair Worm, Gordius Sp ISSN (Print) 0023-4001 ISSN (Online) 1738-0006 Korean J Parasitol Vol. 53, No. 6: 719-724, December 2015 ▣ CASE REPORT http://dx.doi.org/10.3347/kjp.2015.53.6.719 A Horsehair Worm, Gordius sp. (Nematomorpha: Gordiida), Passed in a Canine Feces Eui-Ju Hong1, Cheolho Sim2, Joon-Seok Chae3, Hyeon-Cheol Kim4, Jinho Park5, Kyoung-Seong Choi6, 7 8 1, Do-Hyeon Yu , Jae-Gyu Yoo , Bae-Keun Park * 1College of Veterinary Medicine, Chungnam National University, Daejeon 35015, Korea; 2Department of Biology, Baylor University, Waco, Texas 76798, USA; 3Laboratory of Veterinary Internal Medicine, BK21 PLUS Program for Creative Veterinary Science Research and College of Veterinary Medicine, Seoul National University, Seoul 03080, Korea; 4College of Veterinary Medicine, Gangwon National University, Chuncheon 24289, Korea; 5College of Veterinary Medicine, Chonbuk National University, Cheongju 28644, Korea; 6College of Ecology and Environmental Science, Kyungpook National University, Sangju 37224, Korea; 7College of Veterinary Medicine, Chonnam National University, Gwangju 61186, Korea; 8Laboratory of Veterinary Clinics, National Institute of Animal Science Rural Development Administration, Gwangju 61186, Korea Abstract: Nematomorpha, horsehair or Gordian worms, include about 300 freshwater species in 22 genera (Gordiida) and 5 marine species in 1 marine genus (Nectonema). They are parasitic in arthropods during their juvenile stage. In the present study, the used gordian worm was found in the feces of a dog (5-month old, male) in July 2014. Following the worm analysis using light and scanning electron microscopes, the morphological classification was re-evaluated with mo- lecular analysis. The worm was determined to be a male worm having a bi-lobed tail and had male gonads in cross sec- tions. It was identified as Gordius sp. (Nematomorpha: Gordiidae) based on the characteristic morphologies of cross sec- tions and areole on the cuticle. DNA analysis on 18S rRNA partial sequence arrangements was also carried out, and the gordiid worm was assumed to be close to the genus Gordius based on a phylogenic tree analysis. Key words: Gordius, horsehair worm, Nematomorpha, dog, Korea INTRODUCTION na in Korea [10-12]. Although the distribution and identifica- tion for gordian worms have been studied, there still remained Juvenile horsehair or gordian worms (Nematomorpha) are a lot of undefined gordian worms. obligate parasites of terrestrial insects and, as adults, are free- This study deals with a Gordius sp. (Nematomorpha: Gordi- living in freshwater sites including lakes, streams, and rivers ida) passed in a canine feces in Korea. For identification of the [1,2]. After the larval stage, adult worms kill and leave the host gordian worm, it was studied by light, scanning, and transmis- for the beginning of the free-living stage [3]. Nematomorpha sion electron microscopes, and the morphological classifica- include about 300 freshwater species in 22 genera (Gordiida) tion was re-evaluated with molecular analysis. and 5 marine species in 1 marine genus (Nectonema) [4]. Even though terrestrial insects act as a host, there are some CASE DESCRIPTION reports on the presence of Nematomorpha in frogs, fishes, birds, and mammals including human beings [3,5]. However, In Nonsan-si, Chungcheongnam-do, a gordian worm was mammalian parasitism of gordian worms is uncommon in passed in the feces of a cat (5-month old, male) which was the literature, although many gordian worms have been iden- alive and wiggling vigorously at that time (Fig. 1). The worm tified in different parts of the world from specimens recovered was placed in lacto-phenol solution (glycerin 20 ml, lactic acid from the mouth, urethra, and anus [6-9]. To date, a total of 9 10 ml, phenol 10 ml, and distilled water 10 ml) for 24 hr and species in 3 genera have been recorded in the gordioidean fau- tentatively identified under a light microscope. For scanning electron microscopy (SEM), the pieces of para- Received 20 March 2015, revised 7 September 2015, accepted 9 September 2015. site was washed 5 times with 0.2 M cacodylate buffer (pH 7.3) • Corresponding author ([email protected]) * and fixed in 2.5% glutaraldehyde, post-fixed in 1% osmium © 2015, Korean Society for Parasitology and Tropical Medicine tetroxide at 4˚C. The specimens were then dehydrated in a This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) graded ethyl alcohol series, dried by a CO2 critical point dryer, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. coated with osmium, and examined by a SEM (S-4800, Hita- 719 720 Korean J Parasitol Vol. 53, No. 6: 719-724, December 2015 A B C Fig. 1. Gross and light microscopic features of Gordius sp. (A) Gross finding of the worm. (B) The rounded calotte. (C) The posterior end. Tail is divided into 2 lobes (arrows). chi, Ibaraki, Japan) at an accelerating voltage of 15 kV. Thermal Cycler (Bio-Rad Laboratories, Hercules, California, For the DNA extraction and amplification, the genomic USA) using EmeraldAmp GT PCR Master Mix (Takara, Shiga, DNA was extracted from the gordian worm by using a Japan) with 1 μl DNA aliquot. The PCR products were next vi- DNeasy® Blood and tissue kit (Qiagen, Alameda, California, sualized via electrophoresis on 1.2% agarose gel, and then pu- USA) according to the manufacturer’s instructions. Several se- rified using QIAquick PCR purification kit (Qiagen). quences from Gordius albopunctatus, Gordius aquaticus, and Gor- For the PCR sequence analysis, amplifications were directly dius paranensis were aligned using Multiple Sequence Align- sequenced using ABI Prism Big Dye terminator (v. 3.0) ready ment (Clustal Omega, http://www.ebi.ac.uk/Tools/msa/clusta- reaction cycle sequencing kits (Applied Biosystems, Foster City, lo/), and then common Gordius primers were designed using California, USA) with the same primers as those used in PCR. the online tool (Primer3input, http://primer3.ut.ee/). An 18S The sequencing reactions were run on a PE Applied Biosys- rRNA region spanning internal transcribed spacer 2 (ITS2) tems 3100 automated sequencer. The sequence data were gene (DNA) was amplified for genomic DNA sequence using aligned by Clustal Omega program (clustal O 1.2.1). A phylo- PCR. The oligonucleotide sequences of primers employed to genetic tree-based sequence analysis was conducted by neigh- detect Gordius 18S rRNA region spanning ITS2 gene (DNA), bor-joining using the blast tree program (http://blast.ncbi. were 5´-GTCGTAACGGGTAACGGAGA-3´ (forward) and nlm.nih.gov/Blast.cgi). 5´-TTTCGGACCAGGAGAATGAC-3´ (reverse). The primer set In gross findings, the body was 19.5 mm in length and 1.0 were designed around 1,165 bp product, variable for all se- mm in diameter (Fig. 1A), and its color was light brown. In quences aligned. Under standard condition such as 95˚C for more details, the anterior end (calotte) was rounded with dark 30 sec, annealing at 60˚C for 30 sec, and extension at 72˚C for color, and the mouth was presented at the center (Fig. 1B), but 1 min, PCR reaction was performed in a MyCycler Personal the white tips were not found on the cuticle. The posterior end Hong et al.: A horsehair worm passed in canine feces 721 A B C D E F Fig. 2. SEM finding ofGordius sp. cuticle. (A) Anterior part of the worm. Note the areoles on the cuticle. (B) The magnified square in (A). Spines are scattered on the anterior end. (C) A single spine. (D) The lateral view of the mid-body. Note the areoles found rarely. (E) The ven- tral view of the mid-body. Spines are not found. (F) Ventral view on the posterior end of a male with V-shaped postcloacal crescent and semicircular row of bristles. Note that the tails are bi-lobed and the inverted V-shaped ridge is containing the bristle. The postcloacal cres- cent (PCC) is located behind the cloaca (arrow). was bi-lobed with blunt lobes, with each lobe about twice as tively. As a PCR amplicon, partial ITS2 sequences (1,097 bp) long as wide (Fig. 1C). The cuticle was smooth and slippery. of the Gordius specimens contained 38 variable sites of com- Using SEM analysis, the cuticle structure was not shown as mon sequence in which belonged to the same clade as G. albo- the elevated (increased or high) cuticular areoles on the sur- punctatus, G. aquaticus, and G. paranensis, respectively. The se- face of the body, but the spines on the cuticles of the anterior quence of Gordius specimens was shown with high similarity portion were sseen (Fig. 2A-C). While hairs were found on the in G. albopunctatus (97.6%), G. aquaticus (97.6%), and G. para- anterior portion, it was difficult to find spines in the mid- nensis (97.1%), respectively. Furthermore, partial ITS2 se- body, as shown in Fig. 2D and E. The cuticular areoles ap- quences of the Gordius specimens reveal the low gap difference peared slightly on the anterior portion. The distinct crescent- of nucleotide in G. albopunctatus (0.7%), G. aquaticus (1.0%), shaped fold was located behind the cloaca, and the inverted V- and G. paranensis (0.8%), respectively. Although 5 DNA re- shaped ridge containing some bristle was anterior to the cloaca gions of Gordius specimens was not matched with above se- (Fig. 2F). Interestingly, male tail lobes were 2 times shorter quences of the 3 Gordius sp., the identification was also sup- than their diameter. The post-cloacal crescent was semicircular, ported by the fact that they belonged to the same clades as with the width of about 200 µm, which was about 50% of the Gordius in the phylogenetic tree based on the used ITS2 rRNA width of the posterior end at the level of the crescent (Fig.
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