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Angiostoma Meets Phasmarhabditis: a Case of Angiostoma Kimmeriense Korol & Spiridonov, 1991

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Angiostoma Meets Phasmarhabditis: a Case of Angiostoma Kimmeriense Korol & Spiridonov, 1991 Russian Journal of Nematology, 2018, 26 (1), 77 – 85 Angiostoma meets Phasmarhabditis: a case of Angiostoma kimmeriense Korol & Spiridonov, 1991 Elena S. Ivanova and Sergei E. Spiridonov Centre of Parasitology, A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii Prospect 33, 119071, Moscow, Russia e-mail: [email protected] Accepted for publication 28 June 2018 Summary. Angiostoma kimmeriense (= A. kimmeriensis) Korol & Spiridonov, 1991 was re-isolated from the snail Oxyhilus sp. in the West Caucasus (Adygea Republic) and characterised morphologically and molecularly. The morphology of the genus Angiostoma Dujardin, 1845 was discussed and vertebrate- associated species suggested to be considered as species insertae sedis based on the head end structure (3 vs 6 lips). Phylogenetic analysis based on partial sequences of three RNA domains (D2-D3 segment of LSU rDNA and ITS rDNA) did not resolve the relationships of A. kimmeriense, as the most similar sequences of these loci were found between members of another gastropod associated genus, Phasmarhabditis Andrássy, 1976. However, such biological traits of A. kimmeriense as its large size, limited number of parasites within the host and the site of infection, point to a parasitic rather than pathogenic/necromenic way of life typical for Phasmarhabditis. Key words: description, D2-D3 LSU sequences, ITS RNA sequences, Mollusca, morphology, morphometrics, phylogeny, taxonomy. The family Angiostomatidae comprises two and 2014 did not reveal the presence of the nematode genera, Angiostoma Dujardin, 1845 with its 18 species, in this or other gastropods examined (Vorobjeva et al., and monotypic Aulacnema Pham Van Luc, Spiridonov 2008; Ivanova et al., 2013). Several species of snails and Wilson, 2005. The representatives of the family collected in Adygea (West Caucasus) were examined are generally associated with terrestrial gastropods but for the presence of nematodes. Oxychilus sp. about 20 four species of Angiostoma have been described from mm in diam. (most probably, O. difficilis) was found vertebrate (amphibian and reptile) hosts. It had been infected by Angiostoma sp. together with two other shown that the gastropod-associated angiostomatids nematode species, Phasmarhabditis sp. and belong to the clade V of Nematoda together with Alloionema sp. Morphological examination of gastropod-associated representatives of Agfa Angiostoma sp. showed that it represents A. Dougherty, 1955 and Phasmarhabditis Andrássy, kimmeriense. Three RNA domains were examined and 1976 (Ross et al., 2010). The position of the partial sequences obtained hereby giving the molecular Angiostoma species from vertebrate hosts remains characteristics of this species. The description of A. unclear as no molecular data for them are yet kimmeriense from the West Caucasus is given together available. As to the gastropod-associated species, only with illustrations. half of species have been molecularly characterised so far. Below we present the molecular-phylogenetic MATERIAL AND METHODS analysis for angiostomatids from gastropods based on the recent discovery of A. kimmeriense. Originally, A. Nematode material. Snails, Oxychilus sp., were kimmeriense Korol & Spiridonov, 1991 (= A. collected at the field research station of the South kimmeriensis in original description, spelled here Federal University in Adygea, North Caucasus, according to the gender of the genus following Russian Federation in June 2016 and April 2018. Ivanova & Wilson, 2009) was recovered from the Each snail collected was found to contain a mixed oesophagus of an endemic snail Oxychilus deilus parasite infection. The mixed infection of (Bourguignat, 1857) in Crimea (Korol & Spiridonov, Phasmarhabditis sp. with Angiostoma sp., 1991). The surveys carried in Crimea in 2008, 2011 Phasmarhabditis sp. and Alloionema sp., © Russian Society of Nematologists, 2018; doi:10.24411/0869-6918-2018-10007 77 E.S. Ivanova & S.E. Spiridonov Phasmarhabditis sp. and unidentified trematodes DESCRIPTION was observed as well as other combinations including more than two parasites. Angiostoma kimmeriense Korol & Spiridonov, 1991 Angiostoma kimmeriense were isolated from the (Figs 1 & 2) snail oesophagus and anterior portions of intestine and preserved as follows: for morphological studies, General. Body long, cylindrical, tapering to both in hot 4-5% formalin, and for molecular studies, by ends, tail short. Cuticle thinly annulated. Lateral freezing at –20°C. Formalin-preserved nematodes field expressed as simple thin band less than 1 µm were then processed to glycerin following the wide (Fig. 2G). method of Seinhorst (1959) and mounted on Anterior portion of head ca 13 µm long and ca permanent slides using the wax ring method. 25-30 µm wide, hemi-spherical, lacking annulations, Measurements and drawings were obtained with slightly offset from body contour. Tissue layer just Nikon Eclipse E200 microscopes with drawing beneath cuticle thickened (ca 3-4 µm thick) and attachments. Illustrations were finalised with a enforced by fine, densely packed fibres arranged WACOM Intuos A4 USB drawing tablet and Adobe perpendicularly to the body surface. Six elevations Illustrator CS5. Abbreviations in the text are: a, b, c, situated at the start of annulated region just beneath c’ – de Man indices; L – body length; V% – the margin of the non-annulated part. Each elevation distance from anterior to vulva as the percentage of bearing a salient papilla of internal circle and the body length; GP – male genital papillae. For the smaller one just posterior to it of external circle. SEM studies, formalin-preserved material was Amphids tiny, located slightly farther back. Mouth dehydrated and dried out at critical point in a aperture triangular, moderately sized. Stoma 4-5 µm Hitachi Critical Point Dryer HCP-1 and coated with wide, ca 15-18 µm long, stoma walls not gold in a S150A sputter coater. Images were taken sclerotised, cylindrical at anterior and expanding at on a Tescan Cam Scan MV 2300. bottom. Each stoma sector at bottom bearing 3 Molecular characterisation and phylogenetic prominent cuticular denticles, one ca 3 µm long and analysis. Individual nematodes identified under other two ca 1.5 µm long. Pharynx long, finely light microscope were used for DNA extraction muscular, club-like. Procorpus two thirds of according to the protocol of Holterman et al. (2006). pharynx length; isthmus moderately narrow, poorly PCR amplification was performed as described by marked; basal bulb as wide as procorpus. The Ivanova & Spiridonov (2017). The partial sequence anterior part of procorpus slightly narrower than of A. kimmeriense D2-D3 expansion segment of middle and posterior parts forming a kind of a collar LSU rDNA was deposited in GenBank under surrounding the posterior half of stoma. Valves in MH627383, and partial ITS rDNA as MH627382. the basal bulb very fine, haustrulum present. Cardia BLAST-search was used to identify sequences large, conical, protruding into intestine lumen. similar to these in NCBI GenBank, which were then The position of a nerve ring varies from anterior used for comparison in phylogenetic analysis. The part of isthmus to anterior part of bulb and the sequences were aligned using the Clustal_X position of an excretory pore from bulb base to two program (Thompson et al., 1997). Subsequently, the body diameters posterior to bulb base. The distance sequences were edited using the Genedoc 2.7 between the nerve ring and the excretory pore is program (Nicholas et al., 1997), to prepare a file for nearly constant and the more anterior position of the the analysis in MEGA5 (Tamura et al., 2011). former corresponds with the similar position for the Phylogenetic trees were obtained using three latter. Excretory duct ca 35-45 µm long leading to different methods (MP – maximum parsimony, NJ – ampoule-like chamber. Intestine with thick walls neighbour joining and ML – maximum likelihood) forming diverticula in some specmens. and pairwise nucleotide differences were calculated. Male. n = 4. L = 3643 ± 593 (3180-4460) µm; a = 38.3 ± 3.7 (35.2-43.3); b = 11.5 ± 0.7 (11.1-12.4); RESULTS c = 60.4 ± 6.9 (51.9-66.1); c’ = 1 ± 0.2 (0.7-1.3); pharynx length = 316 ± 75 (257-400) µm; distance The prevalence of Angiostoma infection was 83% from anterior extremity to nerve ring = 230 ± 34 (10 out of 12) and the mean intensity 6 (3-16) (208-270) µm; distance from anterior extremity to specimens. Morphological examination using light and excretory pore = 305 ± 65 (262-380) µm; tail length scanning microscopy has shown that the discovery = 62 ± 17 (49-86) µm; spicule length measured on represents A. kimmeriense as the specimens from arc = 202 ± 8 (191-211) µm; spicule length Adygea were similar to that in the original description in measured on chord = 186 ± 13 (175-198) µm; metric characteristics and general morphological traits. gubernaculum length = 59 ± 5 (54-66) µm. Stoma 78 Angiostoma kimmeriensis in the West Caucasus Fig. 1. Line drawings of Angiostoma kimmeriense from Adygea. A-C: head (A, female; B, male; C, juvenile female); D, E: anterior end of female with different position of excretory pore; F: female tail; G, H: male tail; I: tail of juvenile female; J: female gonad. Except I, all in lateral position. Scale bars in μm. 79 E.S. Ivanova & S.E. Spiridonov Fig. 2. SEM images of Angiostoma kimmeriense from Adygea. A-C: male head; D: male tail; E: male tail, posterior part; F: posteriormost GP and phasmid; G: cuticle of mid-body region of female; H, I: tail tip of female. Arrow indicating opening of pharyngeal gland (B); reduced lip (C); phasmids (E); GP and phasmid (F); lateral field (H). Scale bars in μm. 16 ± 1 (14-17) µm long and 4-5 µm wide. Cardia ca Except GP 5 & 7, all papillae reaching margin of 10 µm long. Testis narrow (ca 1/4 of body diam.), bursa. Both GP5 and GP7 opened on dorsal side of distal portion of testis contains about 15-20 bursa. GP8 not incorporated into bursa and situated spermatids 15 µm in diam. Vas deferens and closely to tail tip in subventral position.
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